diff --git a/src/renderer/src/components/native-chat/native-chat-composer-drop-scope.test.tsx b/src/renderer/src/components/native-chat/native-chat-composer-drop-scope.test.tsx
index 90029987cf4..73953f509a9 100644
--- a/src/renderer/src/components/native-chat/native-chat-composer-drop-scope.test.tsx
+++ b/src/renderer/src/components/native-chat/native-chat-composer-drop-scope.test.tsx
@@ -32,7 +32,7 @@ const intake = vi.hoisted(() => ({
   readFile: vi.fn(),
   upload: vi.fn()
 }))
-vi.mock('@/store', () => ({ useAppStore: { getState: () => ({}) } }))
+vi.mock('@/store', () => ({ useAppStore: { getState: () => ({ tabsByWorktree: {} }) } }))
 // Keeps the real notice strings so the silent-failure guards assert what users see.
 vi.mock('./native-chat-attachment-upload', async (importOriginal) => ({
   ...(await importOriginal<typeof AttachmentUploadModule>()),
diff --git a/src/renderer/src/components/native-chat/native-chat-external-attachments-destination.test.tsx b/src/renderer/src/components/native-chat/native-chat-external-attachments-destination.test.tsx
new file mode 100644
index 00000000000..2b0fe635187
--- /dev/null
+++ b/src/renderer/src/components/native-chat/native-chat-external-attachments-destination.test.tsx
@@ -0,0 +1,214 @@
+// @vitest-environment happy-dom
+import { act, useRef, useState } from 'react'
+import { createRoot, type Root } from 'react-dom/client'
+import { afterEach, beforeEach, describe, expect, it, vi } from 'vitest'
+import type * as AttachmentUploadModule from './native-chat-attachment-upload'
+import type { NativeChatAttachmentOwner } from './native-chat-attachment-upload'
+import { useNativeChatExternalAttachments } from './use-native-chat-external-attachments'
+import {
+  clearNativeChatAttachmentCacheForTests,
+  useNativeChatComposerAttachments
+} from './use-native-chat-composer-attachments'
+
+const mocks = vi.hoisted(() => {
+  const state: {
+    owner: NativeChatAttachmentOwner
+    remoteTarget: boolean
+    stat: ReturnType<typeof vi.fn>
+    upload: ReturnType<typeof vi.fn>
+    tabsByWorktree: Record<string, { id: string }[]>
+  } = {
+    owner: { kind: 'local' },
+    remoteTarget: false,
+    stat: vi.fn(),
+    upload: vi.fn(),
+    tabsByWorktree: { 'workspace-1': [{ id: 'tab-1' }] }
+  }
+  return state
+})
+vi.mock('@/store', () => ({
+  useAppStore: { getState: () => ({ tabsByWorktree: mocks.tabsByWorktree }) }
+}))
+vi.mock('@/i18n/i18n', () => ({ translate: (_key: string, fallback: string) => fallback }))
+vi.mock('@/runtime/runtime-terminal-inspection', () => ({
+  isRemoteRuntimePtyId: () => mocks.remoteTarget
+}))
+vi.mock('./native-chat-attachment-upload', async (importOriginal) => ({
+  ...(await importOriginal<typeof AttachmentUploadModule>()),
+  resolveNativeChatAttachmentOwner: () => mocks.owner,
+  resolveNativeChatAttachmentOwnerForWorktree: () => mocks.owner,
+  uploadNativeChatAttachmentPaths: mocks.upload
+}))
+
+type Api = ReturnType<typeof useNativeChatExternalAttachments> &
+  ReturnType<typeof useNativeChatComposerAttachments>
+let api: Api | undefined
+let root: Root
+let container: HTMLDivElement
+let composing = true
+
+function Probe({ worktreeId }: { worktreeId?: string }): React.JSX.Element {
+  const [draft, setDraft] = useState('')
+  const [caret, setCaret] = useState(0)
+  const [notice, setNotice] = useState<string | null>(null)
+  const textareaRef = useRef<HTMLTextAreaElement>(null)
+  const attachments = useNativeChatComposerAttachments({
+    attachmentScopeKey: 'drop-test',
+    caret,
+    disabled: false,
+    isComposing: () => composing,
+    resolveTarget: () => ({ ptyId: 'pty-1', settings: { activeRuntimeEnvironmentId: null } }),
+    textareaRef,
+    setCaret,
+    setDraft,
+    setNotice
+  })
+  const external = useNativeChatExternalAttachments({
+    terminalTabId: 'tab-1',
+    structuredWorktreeId: worktreeId,
+    disabled: false,
+    attachResolvedPaths: attachments.attachResolvedPaths,
+    setNotice
+  })
+  api = { ...attachments, ...external }
+  return (
+    <>
+      <textarea ref={textareaRef} />
+      <output data-draft>{draft}</output>
+      <output data-notice>{notice}</output>
+    </>
+  )
+}
+
+function latest(): Api {
+  if (!api) {
+    throw new Error('Attachment probe did not render')
+  }
+  return api
+}
+
+async function render(worktreeId?: string): Promise<void> {
+  await act(async () => root.render(<Probe worktreeId={worktreeId} />))
+}
+
+beforeEach(() => {
+  api = undefined
+  composing = true
+  mocks.owner = { kind: 'local' }
+  mocks.remoteTarget = false
+  mocks.stat.mockReset().mockResolvedValue(undefined)
+  mocks.upload.mockReset().mockResolvedValue(['/remote/file.txt'])
+  mocks.tabsByWorktree = { 'workspace-1': [{ id: 'tab-1' }] }
+  vi.stubGlobal('api', { fs: { stat: mocks.stat } })
+  container = document.createElement('div')
+  document.body.append(container)
+  root = createRoot(container)
+})
+
+afterEach(() => {
+  act(() => root.unmount())
+  container.remove()
+  clearNativeChatAttachmentCacheForTests()
+  vi.unstubAllGlobals()
+})
+
+describe('OS attachment destination through input-method composition', () => {
+  it.each(['workspace', 'host', 'ssh-generation', 'terminal-workspace'])(
+    'refuses queued files after the %s changes',
+    async (change) => {
+      if (change === 'ssh-generation') {
+        mocks.owner = {
+          kind: 'ssh',
+          connectionId: 'ssh-1',
+          worktreePath: '/remote',
+          expectedExecutionHostId: 'ssh:ssh-1',
+          expectedSshTargetId: 'ssh-1',
+          expectedSshConnectionGeneration: 1
+        }
+      }
+      await render(change === 'terminal-workspace' ? undefined : 'workspace-1')
+      await act(async () => latest().attachExternalPaths(['/local/file.txt', '/local/image.png']))
+      expect(container.querySelector('[data-draft]')?.textContent).toBe('')
+      if (change === 'workspace') {
+        await render('workspace-2')
+      }
+      if (change === 'host') {
+        mocks.owner = { kind: 'runtime' }
+      }
+      if (change === 'ssh-generation' && mocks.owner.kind === 'ssh') {
+        mocks.owner = { ...mocks.owner, expectedSshConnectionGeneration: 2 }
+      }
+      if (change === 'terminal-workspace') {
+        mocks.tabsByWorktree = { 'workspace-1': [] }
+      }
+      composing = false
+      act(() => latest().flushPendingAttachments())
+      expect(container.querySelector('[data-draft]')?.textContent).toBe('')
+      expect(latest().imageAttachments).toEqual([])
+      expect(container.querySelector('[data-notice]')?.textContent).toBe(
+        'This workspace changed hosts while attaching — drop the files again.'
+      )
+    }
+  )
+
+  it('attaches an unchanged queued OS destination normally', async () => {
+    await render('workspace-1')
+    await act(async () => latest().attachExternalPaths(['/local/file.txt']))
+    composing = false
+    act(() => latest().flushPendingAttachments())
+    expect(container.querySelector('[data-draft]')?.textContent).toBe('@/local/file.txt ')
+  })
+
+  it('refuses an obsolete SSH drop and attaches the retry once during the same composition', async () => {
+    mocks.owner = {
+      kind: 'ssh',
+      connectionId: 'ssh-1',
+      worktreePath: '/remote',
+      expectedExecutionHostId: 'ssh:ssh-1',
+      expectedSshTargetId: 'ssh-1',
+      expectedSshConnectionGeneration: 1
+    }
+    mocks.upload
+      .mockResolvedValueOnce(['/remote/a.txt', '/remote/a.png'])
+      .mockResolvedValueOnce(['/remote/b.txt', '/remote/b.png'])
+    await render('workspace-1')
+    await act(async () => latest().attachExternalPaths(['/local/a.txt', '/local/a.png']))
+    mocks.owner = { ...mocks.owner, expectedSshConnectionGeneration: 2 }
+    await act(async () => latest().attachExternalPaths(['/local/b.txt', '/local/b.png']))
+    expect(container.querySelector('[data-draft]')?.textContent).toBe('')
+    composing = false
+    act(() => {
+      latest().flushPendingAttachments()
+      latest().flushPendingAttachments()
+    })
+    expect(container.querySelector('[data-draft]')?.textContent).toBe('@/remote/b.txt ')
+    expect(latest().imageAttachments).toEqual([
+      expect.objectContaining({ path: '/remote/b.png', connectionId: 'ssh-1' })
+    ])
+    expect(container.querySelector('[data-notice]')?.textContent).toBe(
+      'This workspace changed hosts while attaching — drop the files again.'
+    )
+  })
+
+  it.each([true, false])(
+    'keeps the workspace-file exemption off OS drops (queued=$queued)',
+    async (queued) => {
+      composing = queued
+      await render('workspace-1')
+      if (!queued) {
+        mocks.remoteTarget = true
+      }
+      await act(async () => latest().attachExternalPaths(['/local/file.txt', '/local/image.png']))
+      if (queued) {
+        mocks.remoteTarget = true
+        composing = false
+        act(() => latest().flushPendingAttachments())
+      }
+      expect(container.querySelector('[data-draft]')?.textContent).toBe('')
+      expect(latest().imageAttachments).toEqual([])
+      expect(container.querySelector('[data-notice]')?.textContent).toBe(
+        'Local attachments are not available for remote sessions.'
+      )
+    }
+  )
+})
diff --git a/src/renderer/src/components/native-chat/native-chat-resolved-path-ownership.ts b/src/renderer/src/components/native-chat/native-chat-resolved-path-ownership.ts
index 86290338167..fa9af1624ba 100644
--- a/src/renderer/src/components/native-chat/native-chat-resolved-path-ownership.ts
+++ b/src/renderer/src/components/native-chat/native-chat-resolved-path-ownership.ts
@@ -2,6 +2,8 @@ import { translate } from '@/i18n/i18n'
 import type { NativeChatAttachmentOwner } from './native-chat-attachment-upload'
 
 export type NativeChatResolvedPathOptions = {
+  /** Revalidates the destination without granting workspace-file provenance. */
+  destinationIsCurrent?: () => boolean
   /** Revalidates internal path ownership when an IME-delayed attachment is applied. */
   targetOwnerIsCurrent?: () => boolean
 }
diff --git a/src/renderer/src/components/native-chat/use-native-chat-external-attachments.test.tsx b/src/renderer/src/components/native-chat/use-native-chat-external-attachments.test.tsx
index c72ab81f475..a5d2abc0b31 100644
--- a/src/renderer/src/components/native-chat/use-native-chat-external-attachments.test.tsx
+++ b/src/renderer/src/components/native-chat/use-native-chat-external-attachments.test.tsx
@@ -5,6 +5,7 @@ import { createRoot, type Root } from 'react-dom/client'
 import type * as AttachmentUploadModule from './native-chat-attachment-upload'
 
 const mocks = vi.hoisted(() => ({
+  storeState: { tabsByWorktree: { 'worktree-1': [{ id: 'tab-1' }] } },
   stat: vi.fn(),
   resolveNativeChatAttachmentOwner: vi.fn(),
   resolveNativeChatAttachmentOwnerForWorktree: vi.fn(),
@@ -12,7 +13,7 @@ const mocks = vi.hoisted(() => ({
 }))
 
 vi.mock('@/store', () => ({
-  useAppStore: { getState: () => ({}) }
+  useAppStore: { getState: () => mocks.storeState }
 }))
 
 // Real notice strings, so the tests below assert what a user would actually read
@@ -140,7 +141,9 @@ describe('useNativeChatExternalAttachments', () => {
       filePath: '/local/a.txt',
       access: { kind: 'user-file' }
     })
-    expect(attachResolvedPaths).toHaveBeenCalledWith(['/local/a.txt'])
+    expect(attachResolvedPaths).toHaveBeenCalledWith(['/local/a.txt'], undefined, {
+      destinationIsCurrent: expect.any(Function)
+    })
     expect(mocks.uploadNativeChatAttachmentPaths).not.toHaveBeenCalled()
   })
 
@@ -181,10 +184,11 @@ describe('useNativeChatExternalAttachments', () => {
     expect(attachResolvedPaths).not.toHaveBeenCalled()
     expect(mocks.stat).toHaveBeenCalledTimes(1)
     await act(async () => fileCheck.resolve())
-    expect(attachResolvedPaths).toHaveBeenCalledExactlyOnceWith([
-      '/external/a.png',
-      '/external/c.png'
-    ])
+    expect(attachResolvedPaths).toHaveBeenCalledExactlyOnceWith(
+      ['/external/a.png', '/external/c.png'],
+      undefined,
+      { destinationIsCurrent: expect.any(Function) }
+    )
     expect(mocks.stat).toHaveBeenCalledTimes(3)
   })
 
@@ -329,7 +333,9 @@ describe('useNativeChatExternalAttachments', () => {
       expectedSshTargetId: 'conn-1',
       expectedSshConnectionGeneration: 4
     })
-    expect(attachResolvedPaths).toHaveBeenCalledWith(['/remote/wt/.orca/drops/a.txt'], 'conn-1')
+    expect(attachResolvedPaths).toHaveBeenCalledWith(['/remote/wt/.orca/drops/a.txt'], 'conn-1', {
+      destinationIsCurrent: expect.any(Function)
+    })
     expect(mocks.stat).not.toHaveBeenCalled()
   })
 
@@ -362,8 +368,12 @@ describe('useNativeChatExternalAttachments', () => {
     })
 
     expect(attachResolvedPaths.mock.calls).toEqual([
-      [['/remote/wt/.orca/drops/b.txt', '/remote/wt/.orca/drops/b.txt'], 'conn-1'],
-      [['/remote/wt/.orca/drops/a.txt'], 'conn-1']
+      [
+        ['/remote/wt/.orca/drops/b.txt', '/remote/wt/.orca/drops/b.txt'],
+        'conn-1',
+        { destinationIsCurrent: expect.any(Function) }
+      ],
+      [['/remote/wt/.orca/drops/a.txt'], 'conn-1', { destinationIsCurrent: expect.any(Function) }]
     ])
   })
 
diff --git a/src/renderer/src/components/native-chat/use-native-chat-external-attachments.ts b/src/renderer/src/components/native-chat/use-native-chat-external-attachments.ts
index 5a0189622a4..b23318be314 100644
--- a/src/renderer/src/components/native-chat/use-native-chat-external-attachments.ts
+++ b/src/renderer/src/components/native-chat/use-native-chat-external-attachments.ts
@@ -1,7 +1,10 @@
 import { useCallback, useLayoutEffect, useRef } from 'react'
 import { useAppStore } from '@/store'
 import { NATIVE_FILE_DROP_MAX_PATHS } from '../../../../shared/native-file-drop'
-import { nativeChatAttachmentOwnerUnchanged } from './native-chat-resolved-path-ownership'
+import {
+  nativeChatAttachmentOwnerUnchanged,
+  type NativeChatResolvedPathOptions
+} from './native-chat-resolved-path-ownership'
 import {
   nativeChatAttachmentOwnerChangedNotice,
   nativeChatAttachmentUnreadableNotice,
@@ -14,6 +17,7 @@ import {
   type NativeChatAttachmentOwner
 } from './native-chat-attachment-upload'
 import { userNamedFileAccess } from '@/lib/local-file-access'
+import { findTerminalTabWorktreeId } from './native-chat-file-link'
 
 export type UseNativeChatExternalAttachmentsArgs = {
   terminalTabId: string
@@ -21,7 +25,11 @@ export type UseNativeChatExternalAttachmentsArgs = {
   /** Live composer-disabled state; read at await-resume via a ref so a flip
    *  mid-upload doesn't attach into a guarded composer. */
   disabled: boolean
-  attachResolvedPaths: (paths: string[], connectionId?: string | null) => void
+  attachResolvedPaths: (
+    paths: string[],
+    connectionId?: string | null,
+    options?: NativeChatResolvedPathOptions
+  ) => void
   setNotice: (notice: string | null) => void
 }
 
@@ -95,10 +103,18 @@ export function useNativeChatExternalAttachments({
       // the silent-failure complaint in #15782. Only a disabled composer stays
       // quiet — it is being torn down or guarded, and has no notice surface.
       const capturedWorkspace = workspaceRef.current
+      const currentWorktreeId = (): string | null =>
+        workspaceRef.current.structuredWorktreeId ??
+        findTerminalTabWorktreeId(
+          useAppStore.getState().tabsByWorktree,
+          workspaceRef.current.terminalTabId
+        )
+      const capturedWorktreeId = currentWorktreeId()
       // Both halves matter: a moved tab can land on a workspace that reports the
       // same owner kind, and the owner alone would call that unchanged.
       const ownerStillCurrent = (): boolean =>
         isSameComposerWorkspace(capturedWorkspace, workspaceRef.current) &&
+        capturedWorktreeId === currentWorktreeId() &&
         nativeChatAttachmentOwnerUnchanged(owner, resolveAttachmentOwner())
       if (owner.kind !== 'ssh') {
         void (async () => {
@@ -129,7 +145,7 @@ export function useNativeChatExternalAttachments({
             setNotice(nativeChatAttachmentUnreadableNotice())
             return
           }
-          attachResolvedPaths(readablePaths)
+          attachResolvedPaths(readablePaths, undefined, { destinationIsCurrent: ownerStillCurrent })
         })()
         return
       }
@@ -148,7 +164,9 @@ export function useNativeChatExternalAttachments({
           setNotice(nativeChatAttachmentOwnerChangedNotice())
           return
         }
-        attachResolvedPaths(remotePaths, owner.connectionId)
+        attachResolvedPaths(remotePaths, owner.connectionId, {
+          destinationIsCurrent: ownerStillCurrent
+        })
       })()
     },
     [attachResolvedPaths, resolveAttachmentOwner, setNotice]
diff --git a/src/renderer/src/components/native-chat/use-native-chat-resolved-path-attachments.ts b/src/renderer/src/components/native-chat/use-native-chat-resolved-path-attachments.ts
index 7bc6a042abc..47af01ccb85 100644
--- a/src/renderer/src/components/native-chat/use-native-chat-resolved-path-attachments.ts
+++ b/src/renderer/src/components/native-chat/use-native-chat-resolved-path-attachments.ts
@@ -4,6 +4,7 @@ import { NATIVE_FILE_DROP_MAX_PATHS } from '../../../../shared/native-file-drop'
 import { formatNativeChatFileReference } from './native-chat-composer-target'
 import type { NativeChatComposerInput } from './native-chat-composer-input'
 import { isNativeChatImageAttachmentPath } from './native-chat-image-paste'
+import { nativeChatAttachmentOwnerChangedNotice } from './native-chat-attachment-upload'
 import {
   nativeChatWorkspaceAttachmentMismatchNotice,
   type NativeChatResolvedPathOptions
@@ -12,8 +13,7 @@ import {
 type ResolvedAttachmentPath = {
   path: string
   connectionId?: string | null
-  targetOwnerIsCurrent?: () => boolean
-}
+} & NativeChatResolvedPathOptions
 
 type Args = {
   appendImageAttachments: (paths: { path: string; connectionId?: string | null }[]) => void
@@ -48,14 +48,14 @@ export function useNativeChatResolvedPathAttachments({
   disabledRef: RefObject<boolean>
   flushPendingAttachments: () => void
 } {
-  const pendingResolvedPathsRef = useRef<ResolvedAttachmentPath[]>([])
+  const pendingResolvedBatchesRef = useRef<ResolvedAttachmentPath[][]>([])
   const pendingPathLimitRejectedRef = useRef(false)
   const disabledRef = useRef(disabled)
 
   useLayoutEffect(() => {
     disabledRef.current = disabled
     if (disabled) {
-      pendingResolvedPathsRef.current = []
+      pendingResolvedBatchesRef.current = []
       pendingPathLimitRejectedRef.current = false
     }
   }, [disabled])
@@ -78,15 +78,24 @@ export function useNativeChatResolvedPathAttachments({
     [caret, setCaret, setDraft, textareaRef]
   )
 
-  const applyResolvedPaths = useCallback(
-    (resolvedPaths: ResolvedAttachmentPath[], focus: boolean, preserveNotice = false) => {
-      if (resolvedPaths.length === 0) {
-        return
+  const resolvedBatchIsCurrent = useCallback(
+    (resolvedPaths: ResolvedAttachmentPath[]): boolean => {
+      if (resolvedPaths.some(({ destinationIsCurrent }) => destinationIsCurrent?.() === false)) {
+        setNotice(nativeChatAttachmentOwnerChangedNotice())
+        return false
       }
-      // A failed ownership verdict refuses the whole completion (see the limit
-      // rejection below): an ordered batch is never partially applied.
       if (resolvedPaths.some(({ targetOwnerIsCurrent }) => targetOwnerIsCurrent?.() === false)) {
         setNotice(nativeChatWorkspaceAttachmentMismatchNotice())
+        return false
+      }
+      return true
+    },
+    [setNotice]
+  )
+
+  const applyResolvedPaths = useCallback(
+    (resolvedPaths: ResolvedAttachmentPath[], focus: boolean, preserveNotice = false) => {
+      if (resolvedPaths.length === 0 || !resolvedBatchIsCurrent(resolvedPaths)) {
         return
       }
       // Ownership is per path, so the verdict is too: a queued batch can mix a
@@ -128,6 +137,7 @@ export function useNativeChatResolvedPathAttachments({
       attachmentTargetBlocked,
       insertFileReferences,
       noteAttachmentTargetBlocked,
+      resolvedBatchIsCurrent,
       setNotice,
       textareaRef
     ]
@@ -142,6 +152,10 @@ export function useNativeChatResolvedPathAttachments({
       if (paths.length === 0 || disabledRef.current) {
         return
       }
+      if (options.destinationIsCurrent?.() === false) {
+        setNotice(nativeChatAttachmentOwnerChangedNotice())
+        return
+      }
       const targetOwnerIsCurrent = options.targetOwnerIsCurrent?.()
       if (targetOwnerIsCurrent === false) {
         setNotice(nativeChatWorkspaceAttachmentMismatchNotice())
@@ -152,7 +166,11 @@ export function useNativeChatResolvedPathAttachments({
         return
       }
       if (isComposing()) {
-        if (paths.length > NATIVE_FILE_DROP_MAX_PATHS - pendingResolvedPathsRef.current.length) {
+        const pendingCount = pendingResolvedBatchesRef.current.reduce(
+          (count, batch) => count + batch.length,
+          0
+        )
+        if (paths.length > NATIVE_FILE_DROP_MAX_PATHS - pendingCount) {
           // Reject the whole completion so ordered path batches are never partially applied.
           pendingPathLimitRejectedRef.current = true
           setNotice(
@@ -163,11 +181,11 @@ export function useNativeChatResolvedPathAttachments({
           )
           return
         }
-        pendingResolvedPathsRef.current.push(
-          ...paths.map((path) => ({
+        pendingResolvedBatchesRef.current.push(
+          paths.map((path) => ({
             path,
             connectionId,
-            targetOwnerIsCurrent: options.targetOwnerIsCurrent
+            ...options
           }))
         )
         return
@@ -176,7 +194,7 @@ export function useNativeChatResolvedPathAttachments({
         paths.map((path) => ({
           path,
           connectionId,
-          targetOwnerIsCurrent: options.targetOwnerIsCurrent
+          ...options
         })),
         true
       )
@@ -191,15 +209,22 @@ export function useNativeChatResolvedPathAttachments({
   )
 
   const flushPendingAttachments = useCallback(() => {
-    const paths = pendingResolvedPathsRef.current
-    const preserveNotice = pendingPathLimitRejectedRef.current
-    pendingResolvedPathsRef.current = []
+    const batches = pendingResolvedBatchesRef.current
+    let preserveNotice = pendingPathLimitRejectedRef.current
+    pendingResolvedBatchesRef.current = []
     pendingPathLimitRejectedRef.current = false
-    if (paths.length === 0 || disabledRef.current) {
+    if (batches.length === 0 || disabledRef.current) {
       return
     }
+    const paths = batches.flatMap((batch) => {
+      if (resolvedBatchIsCurrent(batch)) {
+        return batch
+      }
+      preserveNotice = true
+      return []
+    })
     applyResolvedPaths(paths, false, preserveNotice)
-  }, [applyResolvedPaths])
+  }, [applyResolvedPaths, resolvedBatchIsCurrent])
 
   return { attachResolvedPaths, disabledRef, flushPendingAttachments }
 }
diff --git a/src/renderer/src/components/terminal-pane/TerminalPaneHeaderOverlay.test.tsx b/src/renderer/src/components/terminal-pane/TerminalPaneHeaderOverlay.test.tsx
index 031e4ff623b..e9db4adc4bf 100644
--- a/src/renderer/src/components/terminal-pane/TerminalPaneHeaderOverlay.test.tsx
+++ b/src/renderer/src/components/terminal-pane/TerminalPaneHeaderOverlay.test.tsx
@@ -1,13 +1,17 @@
 /**
  * @vitest-environment happy-dom
  */
-import { act, createRef, type ReactNode, type RefObject } from 'react'
+import { act, createRef, type ReactNode } from 'react'
 import { createRoot, type Root } from 'react-dom/client'
 import path from 'node:path'
+import { isTerminalLeafId } from '../../../../shared/stable-pane-id'
 import { afterEach, describe, expect, it, vi } from 'vitest'
 import type { ManagedPane, PaneManager } from '@/lib/pane-manager/pane-manager'
 import type { PtyTransport } from './pty-transport'
 import TerminalPaneHeaderOverlay from './TerminalPaneHeaderOverlay'
+import { handleTerminalFileDrop } from './terminal-drop-handler'
+import { resolveNativeFileDropPath } from '../../../../shared/native-file-drop'
+import { encodeWorkspaceFilePaths, WORKSPACE_FILE_PATHS_MIME } from '@/lib/workspace-file-drag'
 
 vi.mock('@/components/ui/tooltip', () => ({
   Tooltip: ({ children }: { children?: ReactNode }) => children,
@@ -22,17 +26,35 @@ vi.mock('@/i18n/i18n', () => ({
       fallback
     )
 }))
+vi.mock('@/store', () => ({
+  useAppStore: {
+    getState: () => ({
+      settings: { activeRuntimeEnvironmentId: null },
+      repos: [{ id: 'repo1', connectionId: null, executionHostId: 'local' }],
+      worktreesByRepo: { repo1: [{ id: 'wt-1', repoId: 'repo1', hostId: 'local', path: '/repo' }] },
+      detectedWorktreesByRepo: {},
+      folderWorkspaces: [],
+      sshConnectionStates: new Map()
+    })
+  }
+}))
+vi.mock('./terminal-input-activity', () => ({ recordTerminalUserInputForLeaf: vi.fn() }))
+
 const mounted: { container: HTMLDivElement; root: Root }[] = []
 
 function makePane(id: number): ManagedPane {
-  const leafId = `leaf-${id}` as ManagedPane['leafId']
+  const leafId = `00000000-0000-4000-8000-00000000000${id}`
+  if (!isTerminalLeafId(leafId)) {
+    throw new Error('Invalid test leaf')
+  }
   return {
     id,
     leafId,
     stablePaneId: leafId,
     container: document.createElement('div'),
     linkTooltip: document.createElement('div'),
-    terminal: {} as ManagedPane['terminal'],
+    // oxlint-disable-next-line typescript/consistent-type-assertions -- SAFETY: Drops only call focus on the test terminal.
+    terminal: { focus: vi.fn() } as unknown as ManagedPane['terminal'],
     fitAddon: {} as ManagedPane['fitAddon'],
     searchAddon: {} as ManagedPane['searchAddon'],
     serializeAddon: {} as ManagedPane['serializeAddon']
@@ -51,7 +73,8 @@ function renderOverlay({
   canContinueAgentSessionInNewSession = false,
   onContinueAgentSessionInNewSession = vi.fn(),
   renameValue = '',
-  renamingPaneId = null
+  renamingPaneId = null,
+  dropSetup
 }: {
   paneTitles: Record<number, string>
   paneCount?: number
@@ -65,13 +88,19 @@ function renderOverlay({
   onContinueAgentSessionInNewSession?: ReturnType<typeof vi.fn>
   renameValue?: string
   renamingPaneId?: number | null
+  dropSetup?: {
+    panes: ManagedPane[]
+    manager: PaneManager
+    transports: Map<number, PtyTransport>
+    activate: (id: number) => void
+  }
 }): {
   container: HTMLDivElement
   onClosePane: ReturnType<typeof vi.fn>
   onRemoveTitle: ReturnType<typeof vi.fn>
   onRenameSubmit: ReturnType<typeof vi.fn>
 } {
-  const panes = [makePane(1), makePane(2)].slice(0, paneCount)
+  const panes = dropSetup?.panes ?? [makePane(1), makePane(2)].slice(0, paneCount)
   const container = document.createElement('div')
   document.body.appendChild(container)
   const root = createRoot(container)
@@ -99,15 +128,15 @@ function renderOverlay({
         paneTitleBackground="transparent"
         terminalContentVisible
         hiddenStartupStyle={{}}
-        managerRef={{ current: null } as RefObject<PaneManager | null>}
-        paneTransportsRef={{ current: new Map() } as RefObject<Map<number, PtyTransport>>}
+        managerRef={{ current: dropSetup?.manager ?? null }}
+        paneTransportsRef={{ current: dropSetup?.transports ?? new Map<number, PtyTransport>() }}
         canContinueAgentSessionInNewSession={canContinueAgentSessionInNewSession}
         onContinueAgentSessionInNewSession={
           onContinueAgentSessionInNewSession as (pane: ManagedPane) => void
         }
         onSplitPane={vi.fn()}
         onBeginPaneDrag={vi.fn()}
-        onActivatePaneTitleInteraction={vi.fn()}
+        onActivatePaneTitleInteraction={dropSetup?.activate ?? vi.fn()}
         onPaneTitleContextMenu={vi.fn()}
         onStartRename={vi.fn()}
         onRemoveTitle={onRemoveTitle as (paneId: number) => void}
@@ -272,3 +301,100 @@ describe('TerminalPaneHeaderOverlay', () => {
     )
   })
 })
+
+function dispatchFileDrag(target: Element, type: 'dragover' | 'drop', internal: boolean): void {
+  const event = new Event(type, { bubbles: true, cancelable: true })
+  Object.defineProperty(event, 'dataTransfer', {
+    value: {
+      types: internal ? [WORKSPACE_FILE_PATHS_MIME] : ['Files'],
+      getData: () => encodeWorkspaceFilePaths(['/repo/file.txt']),
+      dropEffect: 'none'
+    }
+  })
+  target.dispatchEvent(event)
+}
+
+describe('terminal title drop ownership', () => {
+  it.each([
+    { internal: true, dragover: true },
+    { internal: true, dragover: false },
+    { internal: false, dragover: true },
+    { internal: false, dragover: false }
+  ])(
+    'delivers to pane A while B stays active (internal=$internal, dragover=$dragover)',
+    async ({ internal, dragover }) => {
+      const panes = [makePane(1), makePane(2)]
+      let active = panes[1]
+      const activate = vi.fn((id: number) => {
+        active = panes.find((pane) => pane.id === id) ?? active
+      })
+      // oxlint-disable-next-line typescript/consistent-type-assertions -- SAFETY: The drop handler only reads panes and the active pane from this manager.
+      const manager = { getPanes: () => panes, getActivePane: () => active } as PaneManager
+      const sends = [vi.fn(() => true), vi.fn(() => true)]
+      const transports = new Map<number, PtyTransport>()
+      panes.forEach((pane, index) => {
+        // oxlint-disable-next-line typescript/consistent-type-assertions -- SAFETY: This fixture supplies every transport method used by local file drops.
+        const transport = {
+          sendInput: sends[index],
+          getPtyId: () => `pty-${pane.id}`,
+          isConnected: () => true,
+          getExecutionHostId: () => 'local'
+        } as unknown as PtyTransport
+        transports.set(pane.id, transport)
+      })
+      const { container } = renderOverlay({
+        paneTitles: { 1: 'A', 2: 'B' },
+        dropSetup: { panes, manager, transports, activate }
+      })
+      const title = container.querySelector('.pane-title-bar')
+      if (!title) {
+        throw new Error('Title A did not render')
+      }
+      const deliveries: Promise<void>[] = []
+      const legacyCapture = (event: Event): void => {
+        if (internal) {
+          return
+        }
+        event.preventDefault()
+        event.stopPropagation()
+        const entries = event
+          .composedPath()
+          .filter((entry): entry is HTMLElement => entry instanceof HTMLElement)
+          .map((entry) => ({
+            nativeFileDropTarget: entry.dataset.nativeFileDropTarget,
+            terminalTabId: entry.dataset.terminalTabId,
+            terminalPaneLeafId: entry.dataset.terminalPaneLeafId
+          }))
+        const resolution = resolveNativeFileDropPath(entries)
+        if (resolution?.target === 'terminal') {
+          deliveries.push(
+            handleTerminalFileDrop({
+              manager,
+              paneTransports: transports,
+              worktreeId: 'wt-1',
+              tabId: 'tab-1',
+              cwd: '/repo',
+              data: { paths: ['/repo/file.txt'], ...resolution }
+            })
+          )
+        }
+      }
+      document.addEventListener('drop', legacyCapture, true)
+      try {
+        await act(async () => {
+          if (dragover) {
+            dispatchFileDrag(title, 'dragover', internal)
+          }
+          dispatchFileDrag(title, 'drop', internal)
+          await Promise.all(deliveries)
+        })
+      } finally {
+        document.removeEventListener('drop', legacyCapture, true)
+      }
+      expect(sends[0]).toHaveBeenCalledExactlyOnceWith('/repo/file.txt ', 'driving')
+      expect(sends[1]).not.toHaveBeenCalled()
+      expect(activate).not.toHaveBeenCalled()
+      expect(manager.getActivePane()).toBe(panes[1])
+    }
+  )
+})
diff --git a/src/renderer/src/components/terminal-pane/TerminalPaneHeaderOverlay.tsx b/src/renderer/src/components/terminal-pane/TerminalPaneHeaderOverlay.tsx
index 0640f194627..f3b405f6b8e 100644
--- a/src/renderer/src/components/terminal-pane/TerminalPaneHeaderOverlay.tsx
+++ b/src/renderer/src/components/terminal-pane/TerminalPaneHeaderOverlay.tsx
@@ -150,6 +150,7 @@ export default function TerminalPaneHeaderOverlay({
             className="pane-title-bar"
             data-native-file-drop-target="terminal"
             data-terminal-tab-id={tabId}
+            data-terminal-pane-leaf-id={pane.leafId}
             data-pane-prevent-terminal-focus=""
             {...(isActivePane ? { 'data-active-pane': '' } : {})}
             {...(isChromeless ? { 'data-chromeless': '' } : {})}
@@ -158,7 +159,6 @@ export default function TerminalPaneHeaderOverlay({
               title || isEditing ? () => onActivatePaneTitleInteraction(pane.id) : undefined
             }
             onDragOver={(event) => {
-              onActivatePaneTitleInteraction(pane.id)
               if (
                 event.dataTransfer.types.includes(WORKSPACE_FILE_PATH_MIME) ||
                 event.dataTransfer.types.includes(WORKSPACE_FILE_PATHS_MIME)
@@ -176,7 +176,6 @@ export default function TerminalPaneHeaderOverlay({
               }
               event.preventDefault()
               event.stopPropagation()
-              onActivatePaneTitleInteraction(pane.id)
               const manager = managerRef.current
               if (!manager) {
                 return
@@ -188,7 +187,7 @@ export default function TerminalPaneHeaderOverlay({
                 tabId,
                 cwd,
                 dataTransfer: event.dataTransfer,
-                dropTarget: event.target
+                paneLeafId: pane.leafId
               })
             }}
             onContextMenuCapture={(event) => onPaneTitleContextMenu(event, pane.id)}
diff --git a/src/renderer/src/components/terminal-pane/terminal-drop-handler.test.ts b/src/renderer/src/components/terminal-pane/terminal-drop-handler.test.ts
index caa1e1934ce..5c4b99deba9 100644
--- a/src/renderer/src/components/terminal-pane/terminal-drop-handler.test.ts
+++ b/src/renderer/src/components/terminal-pane/terminal-drop-handler.test.ts
@@ -1,45 +1,52 @@
+import { parseExecutionHostId } from '../../../../shared/execution-host'
 import { beforeEach, describe, expect, it, vi } from 'vitest'
 
-const mocks = vi.hoisted(() => ({
-  toastLoading: vi.fn(() => 'toast-1'),
-  toastDismiss: vi.fn(),
-  toastError: vi.fn(),
-  importExternalPathsToRuntime: vi.fn(),
-  resolveDroppedPathsForAgent: vi.fn(),
-  recordTerminalUserInputForLeaf: vi.fn(),
-  storeState: {
-    activeRepoId: 'repo1',
-    activeWorktreeId: 'wt-1',
-    settings: { activeRuntimeEnvironmentId: 'env-1' as string | null },
-    projects: [
-      {
-        id: 'repo1',
-        localWindowsRuntimePreference: { kind: 'inherit-global' as const }
-      }
-    ] as {
-      id: string
-      localWindowsRuntimePreference:
-        | { kind: 'inherit-global' }
-        | { kind: 'windows-host' }
-        | { kind: 'wsl'; distro: string | null }
-    }[],
-    repos: [
-      {
-        id: 'repo1',
-        connectionId: null as string | null,
-        path: '/remote/repo',
-        executionHostId: 'runtime:env-1' as string | null
-      }
-    ],
-    worktreesByRepo: {
-      repo1: [{ id: 'wt-1', repoId: 'repo1', path: '/remote/repo' }]
-    },
-    sshConnectionStates: new Map<
-      string,
-      { remotePlatform?: NodeJS.Platform; connectionGeneration?: number }
-    >()
+const mocks = vi.hoisted(() => {
+  const worktreesByRepo: Record<
+    string,
+    { id: string; repoId: string; path: string; hostId?: string | null }[]
+  > = {
+    repo1: [{ id: 'wt-1', repoId: 'repo1', path: '/remote/repo', hostId: 'runtime:env-1' }]
   }
-}))
+  return {
+    toastLoading: vi.fn(() => 'toast-1'),
+    toastDismiss: vi.fn(),
+    toastError: vi.fn(),
+    importExternalPathsToRuntime: vi.fn(),
+    resolveDroppedPathsForAgent: vi.fn(),
+    recordTerminalUserInputForLeaf: vi.fn(),
+    storeState: {
+      activeRepoId: 'repo1',
+      activeWorktreeId: 'wt-1',
+      settings: { activeRuntimeEnvironmentId: 'env-1' as string | null },
+      projects: [
+        {
+          id: 'repo1',
+          localWindowsRuntimePreference: { kind: 'inherit-global' as const }
+        }
+      ] as {
+        id: string
+        localWindowsRuntimePreference:
+          | { kind: 'inherit-global' }
+          | { kind: 'windows-host' }
+          | { kind: 'wsl'; distro: string | null }
+      }[],
+      repos: [
+        {
+          id: 'repo1',
+          connectionId: null as string | null,
+          path: '/remote/repo',
+          executionHostId: 'runtime:env-1' as string | null
+        }
+      ],
+      worktreesByRepo,
+      sshConnectionStates: new Map<
+        string,
+        { remotePlatform?: NodeJS.Platform; connectionGeneration?: number }
+      >()
+    }
+  }
+})
 
 vi.mock('sonner', () => ({
   toast: {
@@ -76,11 +83,14 @@ function createTerminalTransport(
   ptyId = 'pty-1',
   sendInputAccepted?: ReturnType<typeof vi.fn>
 ) {
+  const host = parseExecutionHostId(mocks.storeState.repos[0]?.executionHostId)
   return {
     sendInput,
     ...(sendInputAccepted ? { sendInputAccepted } : {}),
     getPtyId: vi.fn(() => ptyId),
-    isConnected: vi.fn(() => true)
+    isConnected: vi.fn(() => true),
+    getExecutionHostId: () => (host?.kind === 'runtime' ? 'local' : (host?.id ?? 'local')),
+    getRuntimeEnvironmentId: () => (host?.kind === 'runtime' ? host.environmentId : null)
   }
 }
 
@@ -107,7 +117,14 @@ describe('handleTerminalFileDrop', () => {
       { id: 'repo1', connectionId: null, path: '/remote/repo', executionHostId: 'runtime:env-1' }
     ]
     mocks.storeState.worktreesByRepo = {
-      repo1: [{ id: 'wt-1', repoId: 'repo1', path: '/remote/repo' }]
+      repo1: [
+        {
+          id: 'wt-1',
+          repoId: 'repo1',
+          path: '/remote/repo',
+          hostId: parseExecutionHostId(mocks.storeState.repos[0]?.executionHostId)?.id ?? 'local'
+        }
+      ]
     }
     mocks.storeState.sshConnectionStates = new Map()
   })
@@ -127,10 +144,7 @@ describe('handleTerminalFileDrop', () => {
     const sendInput = vi.fn(() => true)
     const focus = vi.fn()
     const pane = { id: 1, leafId: 'leaf-1', terminal: { focus } }
-    const manager = {
-      getActivePane: () => pane,
-      getPanes: () => [pane]
-    }
+    const manager = { getActivePane: () => pane, getPanes: () => [pane] }
     const paneTransports = new Map([[1, createTerminalTransport(sendInput)]])
 
     await handleTerminalFileDrop({
@@ -139,7 +153,7 @@ describe('handleTerminalFileDrop', () => {
       worktreeId: 'wt-1',
       tabId: 'tab-1',
       cwd: undefined,
-      data: { paths: ['/Users/me/logo.png'], target: 'terminal' }
+      data: { paths: ['/Users/me/logo.png'], target: 'terminal', paneLeafId: 'leaf-1' }
     })
 
     expect(mocks.importExternalPathsToRuntime).toHaveBeenCalledWith(
@@ -184,10 +198,7 @@ describe('handleTerminalFileDrop', () => {
     const sendInput = vi.fn(() => true)
     const focus = vi.fn()
     const pane = { id: 1, leafId: 'leaf-1', terminal: { focus } }
-    const manager = {
-      getActivePane: () => pane,
-      getPanes: () => [pane]
-    }
+    const manager = { getActivePane: () => pane, getPanes: () => [pane] }
     const transport = createTerminalTransport(sendInput)
     transport.getPtyId.mockImplementation(() => ptyId)
 
@@ -197,7 +208,7 @@ describe('handleTerminalFileDrop', () => {
       worktreeId: 'wt-1',
       tabId: 'tab-1',
       cwd: undefined,
-      data: { paths: ['/Users/me/logo.png'], target: 'terminal' }
+      data: { paths: ['/Users/me/logo.png'], target: 'terminal', paneLeafId: 'leaf-1' }
     })
 
     expect(sendInput).not.toHaveBeenCalled()
@@ -208,7 +219,14 @@ describe('handleTerminalFileDrop', () => {
 
   it('uses Windows shell paths for forward-slash UNC runtime worktrees', async () => {
     mocks.storeState.worktreesByRepo = {
-      repo1: [{ id: 'wt-1', repoId: 'repo1', path: '//server/share/repo' }]
+      repo1: [
+        {
+          id: 'wt-1',
+          repoId: 'repo1',
+          path: '//server/share/repo',
+          hostId: parseExecutionHostId(mocks.storeState.repos[0]?.executionHostId)?.id ?? 'local'
+        }
+      ]
     }
     mocks.importExternalPathsToRuntime.mockResolvedValue({
       results: [
@@ -236,7 +254,7 @@ describe('handleTerminalFileDrop', () => {
       worktreeId: 'wt-1',
       tabId: 'tab-1',
       cwd: undefined,
-      data: { paths: ['/Users/me/logo.png'], target: 'terminal' }
+      data: { paths: ['/Users/me/logo.png'], target: 'terminal', paneLeafId: 'leaf-1' }
     })
 
     expect(mocks.importExternalPathsToRuntime).toHaveBeenCalledWith(
@@ -268,6 +286,11 @@ describe('handleTerminalFileDrop', () => {
         executionHostId: 'runtime:owner-runtime'
       }
     ]
+    mocks.storeState.worktreesByRepo = {
+      repo1: [
+        { id: 'wt-1', repoId: 'repo1', path: '/remote/repo', hostId: 'runtime:owner-runtime' }
+      ]
+    }
     mocks.importExternalPathsToRuntime.mockResolvedValue({
       results: [
         {
@@ -294,7 +317,7 @@ describe('handleTerminalFileDrop', () => {
       worktreeId: 'wt-1',
       tabId: 'tab-1',
       cwd: undefined,
-      data: { paths: ['/Users/me/spec.pdf'], target: 'terminal' }
+      data: { paths: ['/Users/me/spec.pdf'], target: 'terminal', paneLeafId: 'leaf-1' }
     })
 
     expect(mocks.importExternalPathsToRuntime).toHaveBeenCalledWith(
@@ -318,6 +341,9 @@ describe('handleTerminalFileDrop', () => {
     mocks.storeState.repos = [
       { id: 'repo1', connectionId: null, path: '/remote/repo', executionHostId: 'local' }
     ]
+    mocks.storeState.worktreesByRepo = {
+      repo1: [{ id: 'wt-1', repoId: 'repo1', path: '/remote/repo', hostId: 'local' }]
+    }
     const sendInput = vi.fn(() => true)
     const focus = vi.fn()
     const pane = { id: 1, leafId: 'leaf-1', terminal: { focus } }
@@ -333,7 +359,7 @@ describe('handleTerminalFileDrop', () => {
       worktreeId: 'wt-1',
       tabId: 'tab-1',
       cwd: undefined,
-      data: { paths: ['/Users/me/spec.pdf'], target: 'terminal' }
+      data: { paths: ['/Users/me/spec.pdf'], target: 'terminal', paneLeafId: 'leaf-1' }
     })
 
     expect(mocks.importExternalPathsToRuntime).not.toHaveBeenCalled()
@@ -358,13 +384,21 @@ describe('handleTerminalFileDrop', () => {
       }
     ]
     mocks.storeState.worktreesByRepo = {
-      repo1: [{ id: 'wt-1', repoId: 'repo1', path: 'C:\\Users\\alice\\repo\\feature' }]
+      repo1: [
+        {
+          id: 'wt-1',
+          repoId: 'repo1',
+          path: 'C:\\Users\\alice\\repo\\feature',
+          hostId: parseExecutionHostId(mocks.storeState.repos[0]?.executionHostId)?.id ?? 'local'
+        }
+      ]
     }
     const sendInput = vi.fn(() => true)
     const focus = vi.fn()
+    const pane = { id: 1, leafId: 'leaf-1', terminal: { focus } }
     const manager = {
-      getActivePane: () => ({ id: 1, leafId: 'leaf-1', terminal: { focus } }),
-      getPanes: () => []
+      getActivePane: () => pane,
+      getPanes: () => [pane]
     }
     const paneTransports = new Map([[1, createTerminalTransport(sendInput)]])
 
@@ -379,7 +413,8 @@ describe('handleTerminalFileDrop', () => {
           'C:\\Users\\alice\\Desktop\\notes one.txt',
           '\\\\wsl.localhost\\Ubuntu\\home\\alice\\repo\\README.md'
         ],
-        target: 'terminal'
+        target: 'terminal',
+        paneLeafId: 'leaf-1'
       }
     })
 
@@ -402,7 +437,14 @@ describe('handleTerminalFileDrop', () => {
       { id: 'repo1', connectionId: null, path: 'C:\\Users\\alice\\repo', executionHostId: 'local' }
     ]
     mocks.storeState.worktreesByRepo = {
-      repo1: [{ id: 'wt-1', repoId: 'repo1', path: 'C:\\Users\\alice\\repo' }]
+      repo1: [
+        {
+          id: 'wt-1',
+          repoId: 'repo1',
+          path: 'C:\\Users\\alice\\repo',
+          hostId: parseExecutionHostId(mocks.storeState.repos[0]?.executionHostId)?.id ?? 'local'
+        }
+      ]
     }
     const sendInput = vi.fn(() => true)
     const pane = { id: 1, leafId: 'leaf-1', terminal: { focus: vi.fn() } }
@@ -413,7 +455,11 @@ describe('handleTerminalFileDrop', () => {
       worktreeId: 'wt-1',
       tabId: 'tab-1',
       cwd: undefined,
-      data: { paths: ['C:\\Users\\alice\\Desktop\\Screenshot 1.png'], target: 'terminal' }
+      data: {
+        paths: ['C:\\Users\\alice\\Desktop\\Screenshot 1.png'],
+        target: 'terminal',
+        paneLeafId: 'leaf-1'
+      }
     })
 
     // Why: the agent runs in Linux, so a Windows-style quote would reach it as a literal.
@@ -428,6 +474,9 @@ describe('handleTerminalFileDrop', () => {
     mocks.storeState.repos = [
       { id: 'repo1', connectionId: null, path: '/repo', executionHostId: 'local' }
     ]
+    mocks.storeState.worktreesByRepo = {
+      repo1: [{ id: 'wt-1', repoId: 'repo1', path: '/repo', hostId: 'local' }]
+    }
     const sendInput = vi.fn(() => true)
     const sendInputAccepted = vi.fn(async () => true)
     const focus = vi.fn()
@@ -446,7 +495,7 @@ describe('handleTerminalFileDrop', () => {
       worktreeId: 'wt-1',
       tabId: 'tab-1',
       cwd: undefined,
-      data: { paths: ['/Users/me/spec.pdf'], target: 'terminal' }
+      data: { paths: ['/Users/me/spec.pdf'], target: 'terminal', paneLeafId: 'leaf-1' }
     })
 
     expect(sendInputAccepted).toHaveBeenCalledWith('/Users/me/spec.pdf ', 'driving')
@@ -461,7 +510,14 @@ describe('handleTerminalFileDrop', () => {
       { id: 'repo1', connectionId: null, path: '/repo', executionHostId: 'local' }
     ]
     mocks.storeState.worktreesByRepo = {
-      repo1: [{ id: 'wt-1', repoId: 'repo1', path: '/repo' }]
+      repo1: [
+        {
+          id: 'wt-1',
+          repoId: 'repo1',
+          path: '/repo',
+          hostId: parseExecutionHostId(mocks.storeState.repos[0]?.executionHostId)?.id ?? 'local'
+        }
+      ]
     }
     const activeSendInput = vi.fn(() => true)
     const targetSendInput = vi.fn(() => true)
@@ -532,7 +588,8 @@ describe('handleTerminalFileDrop', () => {
           'C:\\Users\\Name\\My Project\\file.txt',
           '\\\\wsl.localhost\\Ubuntu-24.04\\home\\user\\repo\\README.md'
         ],
-        target: 'terminal'
+        target: 'terminal',
+        paneLeafId: 'leaf-1'
       }
     })
 
@@ -590,7 +647,11 @@ describe('handleTerminalFileDrop', () => {
       worktreeId: 'wt-1',
       tabId: 'tab-1',
       cwd: undefined,
-      data: { paths: ['C:\\Users\\Name\\My Project\\file.txt'], target: 'terminal' }
+      data: {
+        paths: ['C:\\Users\\Name\\My Project\\file.txt'],
+        target: 'terminal',
+        paneLeafId: 'leaf-1'
+      }
     })
 
     expect(sendInput).not.toHaveBeenCalled()
@@ -609,7 +670,14 @@ describe('handleTerminalFileDrop', () => {
       }
     ]
     mocks.storeState.worktreesByRepo = {
-      repo1: [{ id: 'wt-1', repoId: 'repo1', path: 'C:\\Remote Repo' }]
+      repo1: [
+        {
+          id: 'wt-1',
+          repoId: 'repo1',
+          path: 'C:\\Remote Repo',
+          hostId: parseExecutionHostId(mocks.storeState.repos[0]?.executionHostId)?.id ?? 'local'
+        }
+      ]
     }
     mocks.storeState.sshConnectionStates = new Map([
       ['ssh-win', { remotePlatform: 'win32', connectionGeneration: 4 }]
@@ -633,7 +701,7 @@ describe('handleTerminalFileDrop', () => {
       worktreeId: 'wt-1',
       tabId: 'tab-1',
       cwd: undefined,
-      data: { paths: ['C:\\Users\\Name\\A&B.txt'], target: 'terminal' }
+      data: { paths: ['C:\\Users\\Name\\A&B.txt'], target: 'terminal', paneLeafId: 'leaf-1' }
     })
 
     expect(mocks.resolveDroppedPathsForAgent).toHaveBeenCalledWith({
@@ -660,7 +728,14 @@ describe('handleTerminalFileDrop', () => {
       }
     ]
     mocks.storeState.worktreesByRepo = {
-      repo1: [{ id: 'wt-1', repoId: 'repo1', path: 'C:\\Remote Repo' }]
+      repo1: [
+        {
+          id: 'wt-1',
+          repoId: 'repo1',
+          path: 'C:\\Remote Repo',
+          hostId: parseExecutionHostId(mocks.storeState.repos[0]?.executionHostId)?.id ?? 'local'
+        }
+      ]
     }
     mocks.storeState.sshConnectionStates = new Map([
       ['ssh-win', { remotePlatform: 'win32', connectionGeneration: 4 }]
@@ -679,7 +754,7 @@ describe('handleTerminalFileDrop', () => {
       worktreeId: 'wt-1',
       tabId: 'tab-1',
       cwd: undefined,
-      data: { paths: ['/Users/me/Screenshot 1.png'], target: 'terminal' }
+      data: { paths: ['/Users/me/Screenshot 1.png'], target: 'terminal', paneLeafId: 'leaf-1' }
     })
 
     // Why: agents on Windows keep backslashes, so POSIX escaping would corrupt the path.
@@ -700,7 +775,14 @@ describe('handleTerminalFileDrop', () => {
       }
     ]
     mocks.storeState.worktreesByRepo = {
-      repo1: [{ id: 'wt-1', repoId: 'repo1', path: '/remote/repo' }]
+      repo1: [
+        {
+          id: 'wt-1',
+          repoId: 'repo1',
+          path: '/remote/repo',
+          hostId: parseExecutionHostId(mocks.storeState.repos[0]?.executionHostId)?.id ?? 'local'
+        }
+      ]
     }
     mocks.storeState.sshConnectionStates = new Map([['ssh-stale', { remotePlatform: 'linux' }]])
     const pane = { id: 1, leafId: 'leaf-1', terminal: { focus: vi.fn() } }
@@ -712,7 +794,7 @@ describe('handleTerminalFileDrop', () => {
         worktreeId: 'wt-1',
         tabId: 'tab-1',
         cwd: undefined,
-        data: { paths: ['/local/a.txt'], target: 'terminal' }
+        data: { paths: ['/local/a.txt'], target: 'terminal', paneLeafId: 'leaf-1' }
       })
     ).resolves.toBeUndefined()
 
@@ -733,7 +815,14 @@ describe('handleTerminalFileDrop', () => {
       }
     ]
     mocks.storeState.worktreesByRepo = {
-      repo1: [{ id: 'wt-1', repoId: 'repo1', path: '/remote/repo' }]
+      repo1: [
+        {
+          id: 'wt-1',
+          repoId: 'repo1',
+          path: '/remote/repo',
+          hostId: parseExecutionHostId(mocks.storeState.repos[0]?.executionHostId)?.id ?? 'local'
+        }
+      ]
     }
     mocks.storeState.sshConnectionStates = new Map([
       ['ssh-linux', { remotePlatform: 'linux', connectionGeneration: 5 }]
@@ -757,7 +846,7 @@ describe('handleTerminalFileDrop', () => {
       worktreeId: 'wt-1',
       tabId: 'tab-1',
       cwd: undefined,
-      data: { paths: ["/Users/me/it's here.txt"], target: 'terminal' }
+      data: { paths: ["/Users/me/it's here.txt"], target: 'terminal', paneLeafId: 'leaf-1' }
     })
 
     expect(sendInput).toHaveBeenCalledWith("'/remote/repo/it'\\''s here.txt' ", 'driving')
diff --git a/src/renderer/src/components/terminal-pane/terminal-drop-handler.ts b/src/renderer/src/components/terminal-pane/terminal-drop-handler.ts
index 63ef95a06ac..eef9a6a7f84 100644
--- a/src/renderer/src/components/terminal-pane/terminal-drop-handler.ts
+++ b/src/renderer/src/components/terminal-pane/terminal-drop-handler.ts
@@ -1,8 +1,7 @@
 import { toast } from 'sonner'
 import { translate } from '@/i18n/i18n'
 import { getConnectionId } from '@/lib/connection-context'
-import { getRuntimeEnvironmentIdForWorktree } from '@/lib/worktree-runtime-owner'
-import { useAppStore } from '@/store'
+import { parseExecutionHostId } from '../../../../shared/execution-host'
 import { recordTerminalUserInputForLeaf } from './terminal-input-activity'
 import { readWorkspaceFileDragPaths } from '@/lib/workspace-file-drag'
 import { captureTerminalDropTarget } from './terminal-drop-target'
@@ -24,6 +23,7 @@ export { handleTerminalFileDrop }
 type InternalArgs = Omit<NativeTerminalFileDropArgs, 'data'> & {
   dataTransfer: Pick<DataTransfer, 'getData'>
   dropTarget?: EventTarget | null
+  paneLeafId?: string
 }
 
 export type InternalTerminalFileDropResult =
@@ -43,7 +43,8 @@ export async function handleInternalTerminalFileDrop({
   tabId,
   cwd,
   dataTransfer,
-  dropTarget
+  dropTarget,
+  paneLeafId
 }: InternalArgs): Promise<InternalTerminalFileDropResult> {
   const dragPaths = readWorkspaceFileDragPaths(dataTransfer)
   if (dragPaths.status === 'rejected') {
@@ -56,7 +57,7 @@ export async function handleInternalTerminalFileDrop({
     return { status: 'ignored', reason: 'empty' }
   }
 
-  const pane = resolveInternalTerminalDropPane(manager, dropTarget)
+  const pane = resolveInternalTerminalDropPane(manager, dropTarget, paneLeafId)
   if (!pane) {
     return { status: 'ignored', reason: 'no-pane' }
   }
@@ -66,12 +67,18 @@ export async function handleInternalTerminalFileDrop({
   }
   const dropTargetSnapshot = captureTerminalDropTarget(pane, transport)
 
-  const state = useAppStore.getState()
-  const worktreePath = resolveTerminalDropWorktreePath(worktreeId, cwd) ?? paths[0]
+  const host = parseExecutionHostId(transport.getExecutionHostId?.())
+  const runtimeEnvironmentId =
+    transport.getRuntimeEnvironmentId?.() ?? (host?.kind === 'runtime' ? host.environmentId : null)
+  const worktreePath = resolveTerminalDropWorktreePath(
+    worktreeId,
+    runtimeEnvironmentId ? undefined : cwd,
+    host?.id,
+    runtimeEnvironmentId
+  )
   if (!worktreePath) {
     return { status: 'ignored', reason: 'worktree-unavailable' }
   }
-  const runtimeEnvironmentId = getRuntimeEnvironmentIdForWorktree(state, worktreeId)
   const connectionId = getConnectionId(worktreeId)
   if (!runtimeEnvironmentId && connectionId === undefined) {
     // Why: unresolved connection metadata means we cannot know whether these
diff --git a/src/renderer/src/components/terminal-pane/terminal-drop-internal-handler.test.ts b/src/renderer/src/components/terminal-pane/terminal-drop-internal-handler.test.ts
index cd42929c248..f4851e09363 100644
--- a/src/renderer/src/components/terminal-pane/terminal-drop-internal-handler.test.ts
+++ b/src/renderer/src/components/terminal-pane/terminal-drop-internal-handler.test.ts
@@ -1,42 +1,50 @@
+// @vitest-environment happy-dom
+import { parseExecutionHostId } from '../../../../shared/execution-host'
 import { beforeEach, describe, expect, it, vi } from 'vitest'
 
-const mocks = vi.hoisted(() => ({
-  toastLoading: vi.fn(() => 'toast-1'),
-  toastDismiss: vi.fn(),
-  toastError: vi.fn(),
-  importExternalPathsToRuntime: vi.fn(),
-  resolveDroppedPathsForAgent: vi.fn(),
-  recordTerminalUserInputForLeaf: vi.fn(),
-  storeState: {
-    activeRepoId: 'repo1',
-    activeWorktreeId: 'wt-1',
-    settings: { activeRuntimeEnvironmentId: 'env-1' as string | null },
-    projects: [
-      {
-        id: 'repo1',
-        localWindowsRuntimePreference: { kind: 'inherit-global' as const }
-      }
-    ] as {
-      id: string
-      localWindowsRuntimePreference:
-        | { kind: 'inherit-global' }
-        | { kind: 'windows-host' }
-        | { kind: 'wsl'; distro: string | null }
-    }[],
-    repos: [
-      {
-        id: 'repo1',
-        connectionId: null as string | null,
-        path: '/remote/repo',
-        executionHostId: 'runtime:env-1' as string | null
-      }
-    ],
-    worktreesByRepo: {
-      repo1: [{ id: 'wt-1', repoId: 'repo1', path: '/remote/repo' }]
-    },
-    sshConnectionStates: new Map<string, { remotePlatform?: NodeJS.Platform }>()
+const mocks = vi.hoisted(() => {
+  const worktreesByRepo: Record<
+    string,
+    { id: string; repoId: string; path: string; hostId?: string | null }[]
+  > = {
+    repo1: [{ id: 'wt-1', repoId: 'repo1', path: '/remote/repo', hostId: 'runtime:env-1' }]
   }
-}))
+  return {
+    toastLoading: vi.fn(() => 'toast-1'),
+    toastDismiss: vi.fn(),
+    toastError: vi.fn(),
+    importExternalPathsToRuntime: vi.fn(),
+    resolveDroppedPathsForAgent: vi.fn(),
+    recordTerminalUserInputForLeaf: vi.fn(),
+    storeState: {
+      activeRepoId: 'repo1',
+      activeWorktreeId: 'wt-1',
+      settings: { activeRuntimeEnvironmentId: 'env-1' as string | null },
+      projects: [
+        {
+          id: 'repo1',
+          localWindowsRuntimePreference: { kind: 'inherit-global' as const }
+        }
+      ] as {
+        id: string
+        localWindowsRuntimePreference:
+          | { kind: 'inherit-global' }
+          | { kind: 'windows-host' }
+          | { kind: 'wsl'; distro: string | null }
+      }[],
+      repos: [
+        {
+          id: 'repo1',
+          connectionId: null as string | null,
+          path: '/remote/repo',
+          executionHostId: 'runtime:env-1' as string | null
+        }
+      ],
+      worktreesByRepo,
+      sshConnectionStates: new Map<string, { remotePlatform?: NodeJS.Platform }>()
+    }
+  }
+})
 
 vi.mock('sonner', () => ({
   toast: {
@@ -73,11 +81,14 @@ function createTerminalTransport(
   ptyId = 'pty-1',
   sendInputAccepted?: ReturnType<typeof vi.fn>
 ) {
+  const host = parseExecutionHostId(mocks.storeState.repos[0]?.executionHostId)
   return {
     sendInput,
     ...(sendInputAccepted ? { sendInputAccepted } : {}),
     getPtyId: vi.fn(() => ptyId),
-    isConnected: vi.fn(() => true)
+    isConnected: vi.fn(() => true),
+    getExecutionHostId: () => (host?.kind === 'runtime' ? 'local' : (host?.id ?? 'local')),
+    getRuntimeEnvironmentId: () => (host?.kind === 'runtime' ? host.environmentId : null)
   }
 }
 
@@ -89,7 +100,14 @@ describe('handleInternalTerminalFileDrop', () => {
       { id: 'repo1', connectionId: null, path: '/repo', executionHostId: 'local' }
     ]
     mocks.storeState.worktreesByRepo = {
-      repo1: [{ id: 'wt-1', repoId: 'repo1', path: '/repo' }]
+      repo1: [
+        {
+          id: 'wt-1',
+          repoId: 'repo1',
+          path: '/repo',
+          hostId: parseExecutionHostId(mocks.storeState.repos[0]?.executionHostId)?.id ?? 'local'
+        }
+      ]
     }
     mocks.storeState.sshConnectionStates = new Map()
   })
@@ -97,9 +115,10 @@ describe('handleInternalTerminalFileDrop', () => {
   it('pastes every selected internal file path with shell spacing', async () => {
     const sendInput = vi.fn(() => true)
     const focus = vi.fn()
+    const pane = { id: 1, leafId: 'leaf-1', terminal: { focus } }
     const manager = {
-      getActivePane: () => ({ id: 1, leafId: 'leaf-1', terminal: { focus } }),
-      getPanes: () => []
+      getActivePane: () => pane,
+      getPanes: () => [pane]
     }
     const paths = ['/repo/a.ts', '/repo/my file.ts']
 
@@ -109,6 +128,7 @@ describe('handleInternalTerminalFileDrop', () => {
       worktreeId: 'wt-1',
       tabId: 'tab-1',
       cwd: undefined,
+      paneLeafId: 'leaf-1',
       dataTransfer: {
         getData: (type) =>
           type === WORKSPACE_FILE_PATHS_MIME ? encodeWorkspaceFilePaths(paths) : ''
@@ -148,6 +168,7 @@ describe('handleInternalTerminalFileDrop', () => {
       worktreeId: 'wt-1',
       tabId: 'tab-1',
       cwd: undefined,
+      paneLeafId: 'leaf-1',
       dataTransfer: {
         getData: (type) =>
           type === WORKSPACE_FILE_PATHS_MIME
@@ -170,9 +191,10 @@ describe('handleInternalTerminalFileDrop', () => {
     const sendInput = vi.fn(() => true)
     const sendInputAccepted = vi.fn(async () => true)
     const focus = vi.fn()
+    const pane = { id: 1, leafId: 'leaf-1', terminal: { focus } }
     const manager = {
-      getActivePane: () => ({ id: 1, leafId: 'leaf-1', terminal: { focus } }),
-      getPanes: () => []
+      getActivePane: () => pane,
+      getPanes: () => [pane]
     }
 
     const result = await handleInternalTerminalFileDrop({
@@ -183,6 +205,7 @@ describe('handleInternalTerminalFileDrop', () => {
       worktreeId: 'wt-1',
       tabId: 'tab-1',
       cwd: undefined,
+      paneLeafId: 'leaf-1',
       dataTransfer: {
         getData: (type) =>
           type === WORKSPACE_FILE_PATHS_MIME ? encodeWorkspaceFilePaths(['/repo/a.ts']) : ''
@@ -199,11 +222,15 @@ describe('handleInternalTerminalFileDrop', () => {
   it('does not paste internal paths when connection metadata is not hydrated', async () => {
     mocks.storeState.settings = { activeRuntimeEnvironmentId: null }
     mocks.storeState.repos = []
+    mocks.storeState.worktreesByRepo = {
+      repo1: [{ id: 'wt-1', repoId: 'repo1', path: '/repo', hostId: '' }]
+    }
     const sendInput = vi.fn(() => true)
     const focus = vi.fn()
+    const pane = { id: 1, leafId: 'leaf-1', terminal: { focus } }
     const manager = {
-      getActivePane: () => ({ id: 1, leafId: 'leaf-1', terminal: { focus } }),
-      getPanes: () => []
+      getActivePane: () => pane,
+      getPanes: () => [pane]
     }
 
     const result = await handleInternalTerminalFileDrop({
@@ -212,6 +239,7 @@ describe('handleInternalTerminalFileDrop', () => {
       worktreeId: 'wt-1',
       tabId: 'tab-1',
       cwd: undefined,
+      paneLeafId: 'leaf-1',
       dataTransfer: {
         getData: (type) =>
           type === WORKSPACE_FILE_PATHS_MIME ? encodeWorkspaceFilePaths(['/repo/a.ts']) : ''
@@ -235,13 +263,21 @@ describe('handleInternalTerminalFileDrop', () => {
       }
     ]
     mocks.storeState.worktreesByRepo = {
-      repo1: [{ id: 'wt-1', repoId: 'repo1', path: 'C:\\repo' }]
+      repo1: [
+        {
+          id: 'wt-1',
+          repoId: 'repo1',
+          path: 'C:\\repo',
+          hostId: parseExecutionHostId(mocks.storeState.repos[0]?.executionHostId)?.id ?? 'local'
+        }
+      ]
     }
     const sendInput = vi.fn(() => true)
     const focus = vi.fn()
+    const pane = { id: 1, leafId: 'leaf-1', terminal: { focus } }
     const manager = {
-      getActivePane: () => ({ id: 1, leafId: 'leaf-1', terminal: { focus } }),
-      getPanes: () => []
+      getActivePane: () => pane,
+      getPanes: () => [pane]
     }
 
     const result = await handleInternalTerminalFileDrop({
@@ -250,6 +286,7 @@ describe('handleInternalTerminalFileDrop', () => {
       worktreeId: 'wt-1',
       tabId: 'tab-1',
       cwd: undefined,
+      paneLeafId: 'leaf-1',
       dataTransfer: {
         getData: (type) =>
           type === WORKSPACE_FILE_PATHS_MIME ? encodeWorkspaceFilePaths(['C:\\repo\\a&b.txt']) : ''
@@ -271,14 +308,22 @@ describe('handleInternalTerminalFileDrop', () => {
       }
     ]
     mocks.storeState.worktreesByRepo = {
-      repo1: [{ id: 'wt-1', repoId: 'repo1', path: 'C:\\Remote Repo' }]
+      repo1: [
+        {
+          id: 'wt-1',
+          repoId: 'repo1',
+          path: 'C:\\Remote Repo',
+          hostId: parseExecutionHostId(mocks.storeState.repos[0]?.executionHostId)?.id ?? 'local'
+        }
+      ]
     }
     mocks.storeState.sshConnectionStates = new Map([['ssh-win', { remotePlatform: 'win32' }]])
     const sendInput = vi.fn(() => true)
     const focus = vi.fn()
+    const pane = { id: 1, leafId: 'leaf-1', terminal: { focus } }
     const manager = {
-      getActivePane: () => ({ id: 1, leafId: 'leaf-1', terminal: { focus } }),
-      getPanes: () => []
+      getActivePane: () => pane,
+      getPanes: () => [pane]
     }
 
     const result = await handleInternalTerminalFileDrop({
@@ -287,6 +332,7 @@ describe('handleInternalTerminalFileDrop', () => {
       worktreeId: 'wt-1',
       tabId: 'tab-1',
       cwd: undefined,
+      paneLeafId: 'leaf-1',
       dataTransfer: {
         getData: (type) =>
           type === WORKSPACE_FILE_PATHS_MIME
@@ -312,14 +358,22 @@ describe('handleInternalTerminalFileDrop', () => {
       }
     ]
     mocks.storeState.worktreesByRepo = {
-      repo1: [{ id: 'wt-1', repoId: 'repo1', path: '/remote/repo' }]
+      repo1: [
+        {
+          id: 'wt-1',
+          repoId: 'repo1',
+          path: '/remote/repo',
+          hostId: parseExecutionHostId(mocks.storeState.repos[0]?.executionHostId)?.id ?? 'local'
+        }
+      ]
     }
     mocks.storeState.sshConnectionStates = new Map([['ssh-linux', { remotePlatform: 'linux' }]])
     const sendInput = vi.fn(() => true)
     const focus = vi.fn()
+    const pane = { id: 1, leafId: 'leaf-1', terminal: { focus } }
     const manager = {
-      getActivePane: () => ({ id: 1, leafId: 'leaf-1', terminal: { focus } }),
-      getPanes: () => []
+      getActivePane: () => pane,
+      getPanes: () => [pane]
     }
 
     const result = await handleInternalTerminalFileDrop({
@@ -328,6 +382,7 @@ describe('handleInternalTerminalFileDrop', () => {
       worktreeId: 'wt-1',
       tabId: 'tab-1',
       cwd: undefined,
+      paneLeafId: 'leaf-1',
       dataTransfer: {
         getData: (type) =>
           type === WORKSPACE_FILE_PATHS_MIME
@@ -347,11 +402,7 @@ describe('handleInternalTerminalFileDrop', () => {
     const targetSendInput = vi.fn(() => true)
     const activeFocus = vi.fn()
     const targetFocus = vi.fn()
-    const dropTarget: EventTarget = {
-      addEventListener: vi.fn(),
-      dispatchEvent: vi.fn(() => true),
-      removeEventListener: vi.fn()
-    }
+    const dropTarget = document.createElement('div')
     const activePane = {
       id: 1,
       leafId: 'leaf-active',
@@ -398,9 +449,10 @@ describe('handleInternalTerminalFileDrop', () => {
   it('rejects too many internal paths before writing terminal input', async () => {
     const sendInput = vi.fn(() => true)
     const focus = vi.fn()
+    const pane = { id: 1, leafId: 'leaf-1', terminal: { focus } }
     const manager = {
-      getActivePane: () => ({ id: 1, leafId: 'leaf-1', terminal: { focus } }),
-      getPanes: () => []
+      getActivePane: () => pane,
+      getPanes: () => [pane]
     }
     const paths = Array.from({ length: 257 }, (_value, index) =>
       ['/repo/secret-', String(index), '.txt'].join('')
@@ -412,6 +464,7 @@ describe('handleInternalTerminalFileDrop', () => {
       worktreeId: 'wt-1',
       tabId: 'tab-1',
       cwd: undefined,
+      paneLeafId: 'leaf-1',
       dataTransfer: {
         getData: (type) =>
           type === WORKSPACE_FILE_PATHS_MIME ? encodeWorkspaceFilePaths(paths) : ''
@@ -427,3 +480,32 @@ describe('handleInternalTerminalFileDrop', () => {
     expect(JSON.stringify(mocks.toastError.mock.calls)).not.toContain('secret-')
   })
 })
+
+it('refuses an unresolvable workspace instead of using the dropped path as its root', async () => {
+  mocks.storeState.worktreesByRepo = {}
+  mocks.storeState.settings = { activeRuntimeEnvironmentId: 'focused-runtime' }
+  mocks.storeState.repos = [
+    { id: 'repo1', path: '/repo', executionHostId: 'local', connectionId: null }
+  ]
+  const sendInput = vi.fn(() => true)
+  const focus = vi.fn()
+  const pane = { id: 1, leafId: 'leaf-1', terminal: { focus } }
+  // oxlint-disable-next-line typescript/consistent-type-assertions -- SAFETY: This fixture supplies every manager method used by internal drops.
+  const manager = { getPanes: () => [pane], getActivePane: () => pane } as never
+  const result = await handleInternalTerminalFileDrop({
+    manager,
+    // oxlint-disable-next-line typescript/consistent-type-assertions -- SAFETY: This fixture supplies every transport method used by local drops.
+    paneTransports: new Map([[1, createTerminalTransport(sendInput)]]) as never,
+    worktreeId: 'repo1::/repo',
+    tabId: 'tab-1',
+    cwd: undefined,
+    paneLeafId: 'leaf-1',
+    dataTransfer: {
+      getData: (type) =>
+        type === WORKSPACE_FILE_PATHS_MIME ? encodeWorkspaceFilePaths(['/other/file.txt']) : ''
+    }
+  })
+  expect(result).toEqual({ status: 'ignored', reason: 'worktree-unavailable' })
+  expect(sendInput).not.toHaveBeenCalled()
+  expect(focus).not.toHaveBeenCalled()
+})
diff --git a/src/renderer/src/components/terminal-pane/terminal-drop-local-workspace.test.ts b/src/renderer/src/components/terminal-pane/terminal-drop-local-workspace.test.ts
new file mode 100644
index 00000000000..bb53ff4ab31
--- /dev/null
+++ b/src/renderer/src/components/terminal-pane/terminal-drop-local-workspace.test.ts
@@ -0,0 +1,84 @@
+import { afterEach, beforeEach, describe, expect, it, vi } from 'vitest'
+import { FLOATING_TERMINAL_WORKTREE_ID } from '../../../../shared/constants'
+import { handleInternalTerminalFileDrop, handleTerminalFileDrop } from './terminal-drop-handler'
+import { encodeWorkspaceFilePaths, WORKSPACE_FILE_PATHS_MIME } from '@/lib/workspace-file-drag'
+
+const mocks = vi.hoisted(() => ({
+  state: {
+    settings: { activeRuntimeEnvironmentId: 'focused-runtime' },
+    repos: [],
+    worktreesByRepo: {},
+    detectedWorktreesByRepo: {},
+    folderWorkspaces: [],
+    sshConnectionStates: new Map()
+  },
+  importPaths: vi.fn(),
+  resolvePaths: vi.fn(),
+  recordInput: vi.fn()
+}))
+vi.mock('@/store', () => ({ useAppStore: { getState: () => mocks.state } }))
+vi.mock('@/runtime/runtime-file-client', () => ({
+  importExternalPathsToRuntime: mocks.importPaths
+}))
+vi.mock('./terminal-input-activity', () => ({ recordTerminalUserInputForLeaf: mocks.recordInput }))
+
+afterEach(() => vi.unstubAllGlobals())
+
+describe('local terminals without catalog workspaces', () => {
+  beforeEach(() => {
+    vi.clearAllMocks()
+    vi.stubGlobal('window', { api: { fs: { resolveDroppedPathsForAgent: mocks.resolvePaths } } })
+  })
+
+  it.each(['native', 'internal'])(
+    'preserves %s floating-terminal drops while a runtime is focused',
+    async (lane) => {
+      const sendInput = vi.fn(() => true)
+      const focus = vi.fn()
+      const pane = { id: 1, leafId: 'leaf-1', terminal: { focus } }
+      // oxlint-disable-next-line typescript/consistent-type-assertions -- SAFETY: The handler only enumerates panes and captures their identity.
+      const manager = { getPanes: () => [pane], getActivePane: () => pane } as never
+      // oxlint-disable-next-line typescript/consistent-type-assertions -- SAFETY: The fixture supplies every transport method used by local drops.
+      const paneTransports = new Map([
+        [
+          1,
+          {
+            sendInput,
+            getPtyId: () => 'pty-1',
+            isConnected: () => true,
+            getExecutionHostId: () => 'local'
+          }
+        ]
+      ]) as never
+      const args = {
+        manager,
+        paneTransports,
+        worktreeId: FLOATING_TERMINAL_WORKTREE_ID,
+        tabId: 'floating',
+        cwd: '/terminal/cwd'
+      }
+      if (lane === 'native') {
+        await handleTerminalFileDrop({
+          ...args,
+          data: { target: 'terminal', paneLeafId: 'leaf-1', paths: ['/local/file.txt'] }
+        })
+      } else {
+        const result = await handleInternalTerminalFileDrop({
+          ...args,
+          paneLeafId: 'leaf-1',
+          dataTransfer: {
+            getData: (type) =>
+              type === WORKSPACE_FILE_PATHS_MIME
+                ? encodeWorkspaceFilePaths(['/local/file.txt'])
+                : ''
+          }
+        })
+        expect(result).toEqual({ status: 'pasted', pathCount: 1 })
+      }
+      expect(sendInput).toHaveBeenCalledExactlyOnceWith('/local/file.txt ', 'driving')
+      expect(focus).toHaveBeenCalled()
+      expect(mocks.importPaths).not.toHaveBeenCalled()
+      expect(mocks.resolvePaths).not.toHaveBeenCalled()
+    }
+  )
+})
diff --git a/src/renderer/src/components/terminal-pane/terminal-drop-pane-resolution.test.ts b/src/renderer/src/components/terminal-pane/terminal-drop-pane-resolution.test.ts
new file mode 100644
index 00000000000..17fe8d02b1c
--- /dev/null
+++ b/src/renderer/src/components/terminal-pane/terminal-drop-pane-resolution.test.ts
@@ -0,0 +1,39 @@
+// @vitest-environment happy-dom
+import { describe, expect, it, vi } from 'vitest'
+import type { ManagedPane, PaneManager } from '@/lib/pane-manager/pane-manager'
+import {
+  resolveInternalTerminalDropPane,
+  resolveNativeTerminalDropPane
+} from './terminal-drop-pane-resolution'
+
+describe('terminal drop pane resolution', () => {
+  const container = document.createElement('div')
+  const child = document.createElement('span')
+  container.append(child)
+  // oxlint-disable-next-line typescript/consistent-type-assertions -- SAFETY: Resolution only reads leaf identity and DOM containment.
+  const pane = {
+    id: 1,
+    leafId: '00000000-0000-4000-8000-000000000001',
+    container
+  } as unknown as ManagedPane
+  const getActivePane = vi.fn(() => pane)
+  // oxlint-disable-next-line typescript/consistent-type-assertions -- SAFETY: Resolution only enumerates panes; active-pane access must stay unused.
+  const manager = { getPanes: () => [pane], getActivePane } as unknown as PaneManager
+
+  it('refuses missing or stale native leaves without consulting focus', () => {
+    expect(resolveNativeTerminalDropPane(manager, undefined)).toBeNull()
+    expect(resolveNativeTerminalDropPane(manager, 'stale-leaf')).toBeNull()
+    expect(getActivePane).not.toHaveBeenCalled()
+  })
+
+  it('refuses missing, outside, and stale internal destinations', () => {
+    expect(resolveInternalTerminalDropPane(manager, undefined)).toBeNull()
+    expect(resolveInternalTerminalDropPane(manager, document.createElement('div'))).toBeNull()
+    expect(resolveInternalTerminalDropPane(manager, child, 'stale-leaf')).toBeNull()
+    expect(getActivePane).not.toHaveBeenCalled()
+  })
+
+  it('resolves internal pane content by DOM containment', () => {
+    expect(resolveInternalTerminalDropPane(manager, child)).toBe(pane)
+  })
+})
diff --git a/src/renderer/src/components/terminal-pane/terminal-drop-pane-resolution.ts b/src/renderer/src/components/terminal-pane/terminal-drop-pane-resolution.ts
index b1adefbeaed..f1822b364ce 100644
--- a/src/renderer/src/components/terminal-pane/terminal-drop-pane-resolution.ts
+++ b/src/renderer/src/components/terminal-pane/terminal-drop-pane-resolution.ts
@@ -4,35 +4,29 @@ export function resolveNativeTerminalDropPane(
   manager: PaneManager,
   paneLeafId: string | undefined
 ): ManagedPane | null {
-  const panes = manager.getPanes()
-  if (paneLeafId) {
-    const targetedPane = panes.find((pane) => pane.leafId === paneLeafId)
-    if (targetedPane) {
-      return targetedPane
-    }
-  }
-  return manager.getActivePane() ?? panes[0] ?? null
+  return paneLeafId ? (manager.getPanes().find((pane) => pane.leafId === paneLeafId) ?? null) : null
 }
 
 export function resolveInternalTerminalDropPane(
   manager: PaneManager,
-  dropTarget: EventTarget | null | undefined
+  dropTarget: EventTarget | null | undefined,
+  paneLeafId?: string
 ): ManagedPane | null {
   const panes = manager.getPanes()
+  if (paneLeafId !== undefined) {
+    return resolveNativeTerminalDropPane(manager, paneLeafId)
+  }
   if (dropTarget) {
     const targetedPane = panes.find((pane) => paneContainsDropTarget(pane, dropTarget))
     if (targetedPane) {
       return targetedPane
     }
   }
-  return manager.getActivePane() ?? panes[0] ?? null
+  return null
 }
 
 function paneContainsDropTarget(pane: ManagedPane, dropTarget: EventTarget): boolean {
-  try {
-    // Why: synthetic drag targets are not always DOM Nodes, but browser drops are.
-    return pane.container.contains(dropTarget as Node)
-  } catch {
-    return false
-  }
+  return (
+    typeof Node !== 'undefined' && dropTarget instanceof Node && pane.container.contains(dropTarget)
+  )
 }
diff --git a/src/renderer/src/components/terminal-pane/terminal-drop-runtime-catalog-owner.test.ts b/src/renderer/src/components/terminal-pane/terminal-drop-runtime-catalog-owner.test.ts
new file mode 100644
index 00000000000..4868e269788
--- /dev/null
+++ b/src/renderer/src/components/terminal-pane/terminal-drop-runtime-catalog-owner.test.ts
@@ -0,0 +1,209 @@
+import { afterEach, beforeEach, describe, expect, it, vi } from 'vitest'
+import type { ExecutionHostId } from '../../../../shared/execution-host'
+import { encodeWorkspaceFilePaths, WORKSPACE_FILE_PATHS_MIME } from '@/lib/workspace-file-drag'
+import { handleInternalTerminalFileDrop, handleTerminalFileDrop } from './terminal-drop-handler'
+
+const mocks = vi.hoisted(() => {
+  const worktreesByRepo: Record<
+    string,
+    {
+      id: string
+      repoId: string
+      path: string
+      hostId: ExecutionHostId
+      runtimeOwnerEnvironmentId?: string
+    }[]
+  > = {}
+  const folderWorkspaces: {
+    id: string
+    projectGroupId: string
+    folderPath: string
+    executionHostId: ExecutionHostId
+  }[] = []
+  return {
+    state: {
+      settings: { activeRuntimeEnvironmentId: 'focused-runtime' },
+      repos: [],
+      worktreesByRepo,
+      detectedWorktreesByRepo: {},
+      folderWorkspaces,
+      sshConnectionStates: new Map([['target-1', { connectionGeneration: 99 }]]),
+      sshStateByEnvironment: new Map([
+        [
+          'owner-runtime',
+          { connectionStates: new Map([['target-1', { connectionGeneration: 1 }]]) }
+        ]
+      ])
+    },
+    importPaths: vi.fn(),
+    toastError: vi.fn()
+  }
+})
+vi.mock('@/store', () => ({ useAppStore: { getState: () => mocks.state } }))
+vi.mock('@/runtime/runtime-file-client', () => ({
+  importExternalPathsToRuntime: mocks.importPaths
+}))
+vi.mock('./terminal-input-activity', () => ({ recordTerminalUserInputForLeaf: vi.fn() }))
+vi.mock('sonner', () => ({
+  toast: { loading: vi.fn(), dismiss: vi.fn(), error: mocks.toastError, message: vi.fn() }
+}))
+
+afterEach(() => vi.unstubAllGlobals())
+beforeEach(() => {
+  vi.clearAllMocks()
+  mocks.state.worktreesByRepo = {
+    local: [{ id: 'wt-1', repoId: 'local', path: 'C:\\wrong-local', hostId: 'local' }],
+    remote: [
+      {
+        id: 'wt-1',
+        repoId: 'remote',
+        path: '/owner/workspace',
+        hostId: 'runtime:owner-runtime',
+        runtimeOwnerEnvironmentId: 'owner-runtime'
+      }
+    ]
+  }
+  mocks.state.folderWorkspaces = [
+    {
+      id: 'notes',
+      projectGroupId: 'local',
+      folderPath: 'C:\\wrong-local',
+      executionHostId: 'local'
+    },
+    {
+      id: 'notes',
+      projectGroupId: 'remote',
+      folderPath: '/owner/workspace',
+      executionHostId: 'runtime:owner-runtime'
+    }
+  ]
+  mocks.importPaths.mockResolvedValue({
+    results: [{ status: 'imported', destPath: '/owner/workspace/.orca/drops/file.txt' }]
+  })
+})
+
+async function drop(lane: string, workspaceId: string, executionHostId: ExecutionHostId) {
+  const sendInput = vi.fn(() => true)
+  const pane = { id: 1, leafId: 'leaf-1', terminal: { focus: vi.fn() } }
+  // oxlint-disable-next-line typescript/consistent-type-assertions -- SAFETY: Drops only enumerate this pane and capture its identity.
+  const manager = { getPanes: () => [pane], getActivePane: () => pane } as never
+  const transport = {
+    sendInput,
+    getPtyId: () => 'runtime-pty-1',
+    isConnected: () => true,
+    getExecutionHostId: () => executionHostId,
+    getRuntimeEnvironmentId: () => 'owner-runtime'
+  }
+  // oxlint-disable-next-line typescript/consistent-type-assertions -- SAFETY: The transport supplies every method used by these drop handlers.
+  const paneTransports = new Map([[1, transport]]) as never
+  const args = {
+    manager,
+    paneTransports,
+    worktreeId: workspaceId,
+    tabId: 'tab-1',
+    cwd: '/wrong-cwd'
+  }
+  let result: Awaited<ReturnType<typeof handleInternalTerminalFileDrop>> | undefined
+  if (lane === 'native') {
+    await handleTerminalFileDrop({
+      ...args,
+      data: { target: 'terminal', paneLeafId: 'leaf-1', paths: ['/client/file.txt'] }
+    })
+  } else {
+    result = await handleInternalTerminalFileDrop({
+      ...args,
+      paneLeafId: 'leaf-1',
+      dataTransfer: {
+        getData: (type) =>
+          type === WORKSPACE_FILE_PATHS_MIME
+            ? encodeWorkspaceFilePaths(['/owner/workspace/file with spaces.txt'])
+            : ''
+      }
+    })
+  }
+  return { sendInput, result, transport }
+}
+
+describe.each(['native', 'internal'])('%s runtime terminal catalog ownership', (lane) => {
+  it.each(['worktree', 'folder', 'ssh'])(
+    'resolves a runtime %s without choosing a local duplicate',
+    async (kind) => {
+      const executionHostId = kind === 'ssh' ? 'ssh:target-1' : 'local'
+      if (kind === 'ssh') {
+        mocks.state.worktreesByRepo.remote[0].hostId = 'ssh:target-1'
+        mocks.state.worktreesByRepo.local.push({
+          id: 'wt-1',
+          repoId: 'local',
+          path: 'C:\\wrong-direct-ssh',
+          hostId: 'ssh:target-1'
+        })
+        mocks.state.worktreesByRepo.otherRuntime = [
+          {
+            id: 'wt-1',
+            repoId: 'other',
+            path: 'C:\\wrong-runtime',
+            hostId: 'ssh:target-1',
+            runtimeOwnerEnvironmentId: 'other-runtime'
+          }
+        ]
+      }
+      const workspaceId = kind === 'folder' ? 'folder:notes' : 'wt-1'
+      const { sendInput, result, transport } = await drop(lane, workspaceId, executionHostId)
+      expect(transport.getExecutionHostId()).toBe(executionHostId)
+      expect(transport.getRuntimeEnvironmentId()).toBe('owner-runtime')
+      if (lane === 'native') {
+        expect(mocks.importPaths).toHaveBeenCalledExactlyOnceWith(
+          {
+            settings: { activeRuntimeEnvironmentId: 'owner-runtime' },
+            worktreeId: workspaceId,
+            worktreePath: '/owner/workspace',
+            expectedExecutionHostId: executionHostId,
+            expectedSshTargetId: kind === 'ssh' ? 'target-1' : undefined,
+            expectedSshConnectionGeneration: kind === 'ssh' ? 1 : undefined
+          },
+          ['/client/file.txt'],
+          '/owner/workspace/.orca/drops',
+          { assertCurrent: expect.any(Function) }
+        )
+        expect(sendInput).toHaveBeenCalledExactlyOnceWith(
+          '/owner/workspace/.orca/drops/file.txt ',
+          'driving'
+        )
+      } else {
+        expect(result).toEqual({ status: 'pasted', pathCount: 1 })
+        expect(sendInput).toHaveBeenCalledExactlyOnceWith(
+          "'/owner/workspace/file with spaces.txt' ",
+          'driving'
+        )
+        expect(mocks.importPaths).not.toHaveBeenCalled()
+      }
+      expect(mocks.toastError).not.toHaveBeenCalled()
+    }
+  )
+
+  it.each(['missing-owner', 'wrong-environment', 'wrong-ssh-target'])(
+    'refuses %s instead of borrowing a catalog root',
+    async (mismatch) => {
+      if (mismatch === 'missing-owner') {
+        delete mocks.state.worktreesByRepo.remote
+      } else if (mismatch === 'wrong-environment') {
+        mocks.state.worktreesByRepo.remote[0].hostId = 'ssh:target-1'
+        mocks.state.worktreesByRepo.remote[0].runtimeOwnerEnvironmentId = 'other-runtime'
+      } else {
+        mocks.state.worktreesByRepo.remote[0].hostId = 'ssh:other-target'
+      }
+      const { sendInput, result } = await drop(
+        lane,
+        'wt-1',
+        mismatch === 'missing-owner' ? 'local' : 'ssh:target-1'
+      )
+      expect(sendInput).not.toHaveBeenCalled()
+      expect(mocks.importPaths).not.toHaveBeenCalled()
+      if (lane === 'native') {
+        expect(mocks.toastError).toHaveBeenCalledWith('Worktree path not available.')
+      } else {
+        expect(result).toEqual({ status: 'ignored', reason: 'worktree-unavailable' })
+      }
+    }
+  )
+})
diff --git a/src/renderer/src/components/terminal-pane/terminal-drop-transport-owner.test.ts b/src/renderer/src/components/terminal-pane/terminal-drop-transport-owner.test.ts
new file mode 100644
index 00000000000..8038ee85b12
--- /dev/null
+++ b/src/renderer/src/components/terminal-pane/terminal-drop-transport-owner.test.ts
@@ -0,0 +1,41 @@
+import { describe, expect, it, vi } from 'vitest'
+import { captureTerminalDropTransportOwner } from './terminal-drop-transport-owner'
+
+const mocks = vi.hoisted(() => ({
+  state: {
+    settings: { activeRuntimeEnvironmentId: 'focused-runtime' },
+    sshConnectionStates: new Map([['host-1', { connectionGeneration: 1 }]])
+  }
+}))
+vi.mock('@/store', () => ({ useAppStore: { getState: () => mocks.state } }))
+
+describe('terminal drop transport owner', () => {
+  it('uses the receiving host rather than the focused runtime', () => {
+    const owner = captureTerminalDropTransportOwner({ getExecutionHostId: () => 'local' })
+    expect(owner?.executionHostId).toBe('local')
+    expect(owner?.runtimeEnvironmentId).toBeNull()
+    expect(captureTerminalDropTransportOwner({})).toBeNull()
+  })
+
+  it('captures and rechecks a runtime transport after settings change', () => {
+    let environmentId = 'owner-runtime'
+    const owner = captureTerminalDropTransportOwner({
+      getExecutionHostId: () => 'local',
+      getRuntimeEnvironmentId: () => environmentId
+    })
+    expect(owner?.executionHostId).toBe('local')
+    expect(owner?.expectedExecutionHostId).toBe('local')
+    expect(owner?.runtimeEnvironmentId).toBe('owner-runtime')
+    mocks.state.settings.activeRuntimeEnvironmentId = 'unrelated-runtime'
+    expect(() => owner?.assertCurrent()).not.toThrow()
+    environmentId = 'replacement-runtime'
+    expect(() => owner?.assertCurrent()).toThrow('Terminal upload host changed')
+  })
+
+  it('refuses an SSH attachment after the connection generation changes', () => {
+    const owner = captureTerminalDropTransportOwner({ getExecutionHostId: () => 'ssh:host-1' })
+    expect(owner?.expectedExecutionHostId).toBe('ssh:host-1')
+    mocks.state.sshConnectionStates = new Map([['host-1', { connectionGeneration: 2 }]])
+    expect(() => owner?.assertCurrent()).toThrow('Terminal upload host changed')
+  })
+})
diff --git a/src/renderer/src/components/terminal-pane/terminal-drop-transport-owner.ts b/src/renderer/src/components/terminal-pane/terminal-drop-transport-owner.ts
new file mode 100644
index 00000000000..57bab077d90
--- /dev/null
+++ b/src/renderer/src/components/terminal-pane/terminal-drop-transport-owner.ts
@@ -0,0 +1,46 @@
+import { parseExecutionHostId } from '../../../../shared/execution-host'
+import { captureDirectSshMutationExpectation } from '@/lib/ssh-mutation-expectation'
+import { useAppStore } from '@/store'
+import type { PtyTransport } from './pty-transport'
+
+export function captureTerminalDropTransportOwner(
+  transport: Pick<PtyTransport, 'getExecutionHostId' | 'getRuntimeEnvironmentId'>
+) {
+  const host = parseExecutionHostId(transport.getExecutionHostId?.())
+  if (!host) {
+    return null
+  }
+  const runtimeEnvironmentId =
+    transport.getRuntimeEnvironmentId?.() ?? (host.kind === 'runtime' ? host.environmentId : null)
+  const connectionId = host.kind === 'ssh' ? host.targetId : null
+  const captureExpectation = () =>
+    connectionId
+      ? captureDirectSshMutationExpectation(
+          useAppStore.getState(),
+          connectionId,
+          runtimeEnvironmentId
+        )
+      : { expectedExecutionHostId: 'local' as const }
+  const expectation = captureExpectation()
+  const assertCurrent = (): void => {
+    const current = captureExpectation()
+    if (
+      transport.getExecutionHostId?.() !== host.id ||
+      (transport.getRuntimeEnvironmentId?.() ??
+        (host.kind === 'runtime' ? host.environmentId : null)) !== runtimeEnvironmentId ||
+      current.expectedExecutionHostId !== expectation.expectedExecutionHostId ||
+      ('expectedSshConnectionGeneration' in current &&
+        'expectedSshConnectionGeneration' in expectation &&
+        current.expectedSshConnectionGeneration !== expectation.expectedSshConnectionGeneration)
+    ) {
+      throw new Error('Terminal upload host changed; retry the drop.')
+    }
+  }
+  return {
+    executionHostId: host.id,
+    runtimeEnvironmentId,
+    connectionId,
+    assertCurrent,
+    ...expectation
+  }
+}
diff --git a/src/renderer/src/components/terminal-pane/terminal-drop-worktree-path.test.ts b/src/renderer/src/components/terminal-pane/terminal-drop-worktree-path.test.ts
new file mode 100644
index 00000000000..fa2eea0c9ab
--- /dev/null
+++ b/src/renderer/src/components/terminal-pane/terminal-drop-worktree-path.test.ts
@@ -0,0 +1,58 @@
+import { beforeEach, describe, expect, it, vi } from 'vitest'
+
+const mocks = vi.hoisted(() => {
+  const state: {
+    detectedWorktreesByRepo: Record<string, never>
+    folderWorkspaces: { id: string; folderPath: string; executionHostId: string }[]
+    worktreesByRepo: Record<string, { id: string; path: string; hostId: string }[]>
+  } = { detectedWorktreesByRepo: {}, folderWorkspaces: [], worktreesByRepo: {} }
+  return { state }
+})
+
+vi.mock('@/store', () => ({ useAppStore: { getState: () => mocks.state } }))
+
+import { resolveTerminalDropWorktreePath } from './terminal-drop-worktree-path'
+
+describe('resolveTerminalDropWorktreePath', () => {
+  beforeEach(() => {
+    mocks.state.folderWorkspaces = []
+    mocks.state.worktreesByRepo = {}
+  })
+
+  it('resolves folder workspaces through their recorded host', () => {
+    mocks.state.folderWorkspaces = [
+      { id: 'notes', folderPath: '/folders/notes', executionHostId: 'ssh:host-1' }
+    ]
+    expect(resolveTerminalDropWorktreePath('folder:notes', undefined, 'ssh:host-1')).toBe(
+      '/folders/notes'
+    )
+    expect(resolveTerminalDropWorktreePath('folder:notes', undefined, 'local')).toBeNull()
+  })
+
+  it('resolves the receiving host when the same workspace id exists on two hosts', () => {
+    mocks.state.worktreesByRepo = {
+      local: [{ id: 'wt-1', path: '/local/repo', hostId: 'local' }],
+      remote: [{ id: 'wt-1', path: '/remote/repo', hostId: 'runtime:host-1' }]
+    }
+    expect(resolveTerminalDropWorktreePath('wt-1', undefined, 'runtime:host-1')).toBe(
+      '/remote/repo'
+    )
+    expect(resolveTerminalDropWorktreePath('wt-1', undefined, 'local')).toBe('/local/repo')
+    expect(resolveTerminalDropWorktreePath('wt-1', undefined, 'ssh:unknown')).toBeNull()
+  })
+
+  it('preserves a local terminal cwd without granting remote upload roots', () => {
+    expect(resolveTerminalDropWorktreePath('missing', '/terminal/cwd', 'local')).toBe(
+      '/terminal/cwd'
+    )
+    expect(resolveTerminalDropWorktreePath('missing', '/terminal/cwd', 'ssh:host-1')).toBeNull()
+  })
+
+  it('refuses an unknown workspace or an unknown execution host', () => {
+    expect(resolveTerminalDropWorktreePath('missing', undefined, 'local')).toBeNull()
+    mocks.state.worktreesByRepo = {
+      local: [{ id: 'wt-1', path: '/local/repo', hostId: 'local' }]
+    }
+    expect(resolveTerminalDropWorktreePath('wt-1', undefined, undefined)).toBeNull()
+  })
+})
diff --git a/src/renderer/src/components/terminal-pane/terminal-drop-worktree-path.ts b/src/renderer/src/components/terminal-pane/terminal-drop-worktree-path.ts
index be59370e16d..403ed9c6487 100644
--- a/src/renderer/src/components/terminal-pane/terminal-drop-worktree-path.ts
+++ b/src/renderer/src/components/terminal-pane/terminal-drop-worktree-path.ts
@@ -1,14 +1,42 @@
 import { useAppStore } from '@/store'
+import { findKnownWorktreeById } from '@/store/slices/worktrees/listing/detected-worktree-meta'
+import {
+  parseExecutionHostId,
+  toRuntimeExecutionHostId,
+  type ExecutionHostId
+} from '../../../../shared/execution-host'
+import { resolveExactWorktreeRoute } from '@/lib/worktree-owner-route'
 import { isTerminalDropWindowsPathLike } from './terminal-drop-shell'
 
 export function resolveTerminalDropWorktreePath(
   worktreeId: string,
-  fallbackCwd: string | undefined
+  fallbackCwd: string | undefined,
+  executionHostId: ExecutionHostId | null | undefined,
+  runtimeEnvironmentId?: string | null
 ): string | null {
+  const host = parseExecutionHostId(executionHostId)
+  if (!host) {
+    return null
+  }
+  const environmentId =
+    runtimeEnvironmentId ?? (host.kind === 'runtime' ? host.environmentId : null)
+  // A runtime's physical local host is a different catalog namespace from the client's local host.
+  const catalogHostId = environmentId ? toRuntimeExecutionHostId(environmentId) : host.id
   const state = useAppStore.getState()
-  const allWorktrees = Object.values(state.worktreesByRepo ?? {}).flat()
-  const worktree = allWorktrees.find((w) => w.id === worktreeId)
-  return worktree?.path ?? fallbackCwd ?? null
+  const worktree = findKnownWorktreeById(state, worktreeId, catalogHostId)
+  if (host.kind === 'ssh' && environmentId) {
+    const resolution = worktree && resolveExactWorktreeRoute(state, worktree)
+    if (
+      resolution?.kind !== 'resolved' ||
+      resolution.route.runtimeEnvironmentId !== environmentId ||
+      resolution.route.executionHostId !== host.id
+    ) {
+      return null
+    }
+  } else if (environmentId && parseExecutionHostId(worktree?.hostId)?.kind === 'ssh') {
+    return null
+  }
+  return worktree?.path ?? (catalogHostId === 'local' ? fallbackCwd : null) ?? null
 }
 
 export function joinRuntimeTerminalDropDir(worktreePath: string): string {
diff --git a/src/renderer/src/components/terminal-pane/terminal-native-file-drop.ts b/src/renderer/src/components/terminal-pane/terminal-native-file-drop.ts
index 197a3ffccc2..b43305c82f0 100644
--- a/src/renderer/src/components/terminal-pane/terminal-native-file-drop.ts
+++ b/src/renderer/src/components/terminal-pane/terminal-native-file-drop.ts
@@ -1,5 +1,4 @@
 import { toast } from 'sonner'
-import { getConnectionId } from '@/lib/connection-context'
 import { extractIpcErrorMessage } from '@/lib/ipc-error'
 import { getLocalProjectExecutionRuntimeContext } from '@/lib/local-preflight-context'
 import { CLIENT_PLATFORM } from '@/lib/new-workspace'
@@ -22,12 +21,11 @@ import { writeTerminalDropPathsToCapturedTarget } from './terminal-drop-path-wri
 import { resolveNativeTerminalDropPane } from './terminal-drop-pane-resolution'
 import { getTerminalPasteSshRemotePlatform } from './terminal-paste-ssh-platform'
 import { showTerminalDropWriteFailure } from './terminal-drop-write-failure'
-import { captureDirectSshMutationExpectation } from '@/lib/ssh-mutation-expectation'
 import {
   joinRuntimeTerminalDropDir,
   resolveTerminalDropWorktreePath
 } from './terminal-drop-worktree-path'
-import { captureRuntimeTerminalDropOwner } from './terminal-drop-runtime-owner'
+import { captureTerminalDropTransportOwner } from './terminal-drop-transport-owner'
 
 export type NativeTerminalFileDropArgs = {
   manager: PaneManager
@@ -75,8 +73,13 @@ async function handleNativeTerminalFileDropWithCapturedOwner(
   const dropTarget = captureTerminalDropTarget(pane, transport)
   const state = useAppStore.getState()
   const settings = state.settings
-  const runtimeOwner = captureRuntimeTerminalDropOwner(worktreeId)
-  const worktreePath = resolveTerminalDropWorktreePath(worktreeId, cwd)
+  const owner = captureTerminalDropTransportOwner(transport)
+  const worktreePath = resolveTerminalDropWorktreePath(
+    worktreeId,
+    owner?.runtimeEnvironmentId ? undefined : cwd,
+    owner?.executionHostId,
+    owner?.runtimeEnvironmentId
+  )
   if (!worktreePath) {
     toast.error(
       translate(
@@ -87,7 +90,7 @@ async function handleNativeTerminalFileDropWithCapturedOwner(
     return
   }
 
-  if (runtimeOwner) {
+  if (owner?.runtimeEnvironmentId) {
     await uploadRuntimeDropPaths({
       dataPaths: data.paths,
       dropTarget,
@@ -98,16 +101,13 @@ async function handleNativeTerminalFileDropWithCapturedOwner(
       tabId,
       worktreeId,
       worktreePath,
-      ...runtimeOwner
+      ...owner,
+      runtimeEnvironmentId: owner.runtimeEnvironmentId
     })
     return
   }
 
-  // Why: `getConnectionId` returns `string` (SSH), `null` (local repo found),
-  // or `undefined` (store not hydrated / worktree not found). Treat
-  // `undefined` as an error — otherwise a drop during hydration would
-  // silently paste local paths into a remote shell.
-  const connectionId = getConnectionId(worktreeId)
+  const connectionId = owner?.connectionId
   if (connectionId === undefined) {
     toast.error(
       translate(
@@ -134,6 +134,7 @@ async function handleNativeTerminalFileDropWithCapturedOwner(
       manager,
       paneTransports,
       pane,
+      assertCurrent: owner?.assertCurrent,
       tabId,
       targetShell: localWslDrop ? 'posix' : targetShell,
       worktreePath
@@ -142,8 +143,8 @@ async function handleNativeTerminalFileDropWithCapturedOwner(
   }
 
   await uploadRemoteDropPaths({
+    ...owner,
     connectionId,
-    ...captureDirectSshMutationExpectation(state, connectionId),
     dataPaths: data.paths,
     dropTarget,
     manager,
@@ -278,6 +279,7 @@ async function uploadRemoteDropPaths(
 async function pasteResolvedDropPaths(
   args: NativeDropFlowArgs & { paths: string[]; targetShell: 'posix' | 'windows' }
 ): Promise<void> {
+  args.assertCurrent?.()
   // Why: pane may have unmounted during upload/resolution (tab closed,
   // worktree switched). Re-check before writing so we do not call sendInput
   // on a torn-down PTY.
diff --git a/src/renderer/src/components/terminal-pane/use-terminal-pane-global-effects-file-drop.test.ts b/src/renderer/src/components/terminal-pane/use-terminal-pane-global-effects-file-drop.test.ts
index f9d2de79337..1eacf04cb3d 100644
--- a/src/renderer/src/components/terminal-pane/use-terminal-pane-global-effects-file-drop.test.ts
+++ b/src/renderer/src/components/terminal-pane/use-terminal-pane-global-effects-file-drop.test.ts
@@ -225,20 +225,13 @@ describe('useTerminalPaneGlobalEffects', () => {
     })
   })
 
-  it('keeps handling legacy terminal file drops without a terminal tab id', () => {
-    const { onFileDrop, manager, paneTransports } = useMountForFileDrop()
+  it('refuses terminal file drops without a terminal tab id even in the active tab', () => {
+    const { onFileDrop } = useMountForFileDrop()
 
     const data = { paths: ['/tmp/image.png'], target: 'terminal' }
     onFileDrop(data)
 
-    expect(mocks.handleTerminalFileDrop).toHaveBeenCalledWith({
-      manager,
-      paneTransports,
-      worktreeId: 'wt-1',
-      tabId: 'tab-1',
-      cwd: undefined,
-      data
-    })
+    expect(mocks.handleTerminalFileDrop).not.toHaveBeenCalled()
   })
 
   it('handles terminal file drops for visible unfocused split-group terminals', () => {
diff --git a/src/renderer/src/components/terminal-pane/use-terminal-pane-global-effects.ts b/src/renderer/src/components/terminal-pane/use-terminal-pane-global-effects.ts
index ec693cfe579..f9d749e8b92 100644
--- a/src/renderer/src/components/terminal-pane/use-terminal-pane-global-effects.ts
+++ b/src/renderer/src/components/terminal-pane/use-terminal-pane-global-effects.ts
@@ -297,22 +297,13 @@ export function useTerminalPaneGlobalEffects({
     return () => document.removeEventListener('dictation:insertText', onDictationInsert)
   }, [isActiveRef, managerRef, paneTransportsRef, tabId])
 
-  // Why: visible but unfocused split-group terminals can still receive native
-  // OS drops. Route tab-id-aware payloads to the dropped pane, while legacy
-  // payloads without a tab id keep the old active-terminal-only behavior.
+  // Why: visible, unfocused terminals receive drops only when the payload names their tab.
   useEffect(() => {
     if (!isActive && !isVisible) {
       return
     }
     return window.api.ui.onFileDrop((data) => {
-      if (data.target !== 'terminal') {
-        return
-      }
-      if (data.tabId) {
-        if (data.tabId !== tabId) {
-          return
-        }
-      } else if (!isActive) {
+      if (data.target !== 'terminal' || data.tabId !== tabId) {
         return
       }
       const manager = managerRef.current