diff --git a/src/renderer/src/i18n/locales/en.json b/src/renderer/src/i18n/locales/en.json
index c9fea250709..0c92b681fd4 100644
--- a/src/renderer/src/i18n/locales/en.json
+++ b/src/renderer/src/i18n/locales/en.json
@@ -773,6 +773,9 @@
       },
       "ephemeralVmWorktreeCreation": {
         "sparseCheckoutUnsupported": "Provisioned-root recipes do not support sparse checkout."
+      },
+      "worktreeCreationFlow": {
+        "backgroundStartupOwnerAmbiguous": "Workspace created, but automatic startup was skipped because its host is ambiguous."
       }
     },
     "hooks": {
diff --git a/src/renderer/src/lib/worktree-creation-agent-trust.ts b/src/renderer/src/lib/worktree-creation-agent-trust.ts
new file mode 100644
index 00000000000..96596b913c8
--- /dev/null
+++ b/src/renderer/src/lib/worktree-creation-agent-trust.ts
@@ -0,0 +1,25 @@
+import { TUI_AGENT_CONFIG } from '../../../shared/tui-agent-config'
+import type { WorktreeCreationRequest } from '@/lib/pending-worktree-creation'
+
+export async function preflightWorktreeCreationAgentTrust(
+  request: WorktreeCreationRequest,
+  path: string,
+  connectionId?: string | null
+): Promise<void> {
+  if (!request.agent || !window.api.agentTrust?.markTrusted) {
+    return
+  }
+  const preflight = TUI_AGENT_CONFIG[request.agent].preflightTrust
+  if (!preflight) {
+    return
+  }
+  try {
+    await window.api.agentTrust.markTrusted({
+      preset: preflight,
+      workspacePath: path,
+      ...(connectionId ? { connectionId } : {})
+    })
+  } catch {
+    // Best-effort: the created workspace must remain usable if trust persistence fails.
+  }
+}
diff --git a/src/renderer/src/lib/worktree-creation-flow-agent-trust-preflight.test.ts b/src/renderer/src/lib/worktree-creation-flow-agent-trust-preflight.test.ts
index 928c3dfc87f..8870e7b9702 100644
--- a/src/renderer/src/lib/worktree-creation-flow-agent-trust-preflight.test.ts
+++ b/src/renderer/src/lib/worktree-creation-flow-agent-trust-preflight.test.ts
@@ -3,6 +3,7 @@ import { join } from 'node:path'
 import { describe, expect, it } from 'vitest'
 
 const FLOW_SOURCE = readFileSync(join(__dirname, 'worktree-creation-flow.ts'), 'utf8')
+const TRUST_SOURCE = readFileSync(join(__dirname, 'worktree-creation-agent-trust.ts'), 'utf8')
 
 function sourceBetween(source: string, startPattern: string, endPattern: string): string {
   const start = source.indexOf(startPattern)
@@ -14,23 +15,19 @@ function sourceBetween(source: string, startPattern: string, endPattern: string)
 
 describe('worktree creation flow agent trust preflight', () => {
   it('forwards the repo SSH connection id when pre-marking agent trust', () => {
-    const preflight = sourceBetween(
-      FLOW_SOURCE,
-      'async function preflightAgentTrust',
-      'async function executeWorktreeCreation'
-    )
     const createFlow = sourceBetween(
       FLOW_SOURCE,
       'const backendSpawned = result.startupTerminal?.spawned === true',
       '// `createWorktree` already inserted the real worktree row'
     )
 
-    expect(preflight).toContain('connectionId?: string | null')
-    expect(preflight).toContain('...(connectionId ? { connectionId } : {})')
+    expect(TRUST_SOURCE).toContain('connectionId?: string | null')
+    expect(TRUST_SOURCE).toContain('...(connectionId ? { connectionId } : {})')
     expect(createFlow).toContain('repoConnectionId')
-    expect(createFlow).toContain('repo.id === worktree.repoId')
+    expect(createFlow).toContain('findRepoForHost(trustState.repos, worktree.repoId, {')
+    expect(createFlow).toContain('hostId: worktree.hostId')
     expect(createFlow).toContain(
-      'await preflightAgentTrust(preparedRequest, worktree.path, repoConnectionId)'
+      'await preflightWorktreeCreationAgentTrust(preparedRequest, worktree.path, repoConnectionId)'
     )
   })
 })
diff --git a/src/renderer/src/lib/worktree-creation-flow-host-routing.test.ts b/src/renderer/src/lib/worktree-creation-flow-host-routing.test.ts
new file mode 100644
index 00000000000..71f9a40f106
--- /dev/null
+++ b/src/renderer/src/lib/worktree-creation-flow-host-routing.test.ts
@@ -0,0 +1,143 @@
+import { beforeEach, expect, it, vi } from 'vitest'
+import type { PendingWorktreeCreation, WorktreeCreationRequest } from './pending-worktree-creation'
+
+const mocks = vi.hoisted(() => {
+  const store = {
+    activePendingCreationId: null as string | null,
+    activeView: 'terminal',
+    pendingWorktreeCreations: {} as Record<string, PendingWorktreeCreation>,
+    repos: [],
+    settings: {},
+    beginPendingWorktreeCreation: vi.fn((entry: PendingWorktreeCreation) => {
+      store.pendingWorktreeCreations[entry.creationId] = entry
+      store.activePendingCreationId = entry.creationId
+    }),
+    updatePendingWorktreeCreation: vi.fn(),
+    removePendingWorktreeCreation: vi.fn((creationId: string) => {
+      delete store.pendingWorktreeCreations[creationId]
+    }),
+    createWorktree: vi.fn(),
+    updateWorktreeMeta: vi.fn(),
+    setActivePendingWorktreeCreation: vi.fn(),
+    setActiveView: vi.fn(),
+    setSidebarOpen: vi.fn()
+  }
+  return {
+    store,
+    activateAndRevealWorktree: vi.fn(() => ({ primaryTabId: null })),
+    ensureWorktreeHasInitialTerminal: vi.fn(),
+    toastError: vi.fn(),
+    seedAgentTabState: vi.fn(),
+    ensureAgentStartup: vi.fn(),
+    resolveExplicitRoute: vi.fn<
+      () =>
+        | {
+            kind: 'resolved'
+            route: { executionHostId: 'ssh:requested'; runtimeEnvironmentId: null }
+          }
+        | { kind: 'ambiguous' }
+    >(() => ({
+      kind: 'resolved',
+      route: { executionHostId: 'ssh:requested', runtimeEnvironmentId: null }
+    })),
+    prepareRequestForCreate: vi.fn(
+      async (_creationId: string, request: WorktreeCreationRequest) => request
+    )
+  }
+})
+
+vi.mock('@/store', () => ({ useAppStore: { getState: () => mocks.store } }))
+vi.mock('@/lib/browser-uuid', () => ({ createBrowserUuid: () => 'creation-host-routing' }))
+vi.mock('@/lib/worktree-activation', () => ({
+  activateAndRevealWorktree: mocks.activateAndRevealWorktree,
+  ensureWorktreeHasInitialTerminal: mocks.ensureWorktreeHasInitialTerminal
+}))
+vi.mock('@/lib/ephemeral-vm-worktree-creation', () => ({
+  prepareRequestForCreate: mocks.prepareRequestForCreate,
+  adoptEphemeralVmProvisionedRoot: vi.fn(),
+  attachEphemeralVmRuntimeToWorkspace: vi.fn(),
+  cleanupEphemeralVmRuntimeForFailedCreate: vi.fn()
+}))
+vi.mock('@/lib/worktree-creation-agent-seeds', () => ({
+  seedAgentTabStateAfterWorktreeCreate: mocks.seedAgentTabState
+}))
+vi.mock('@/lib/worktree-operation-route', () => ({
+  resolveExplicitWorktreeOperationRouteResult: mocks.resolveExplicitRoute
+}))
+vi.mock('@/lib/new-workspace', () => ({ ensureAgentStartupInTerminal: mocks.ensureAgentStartup }))
+vi.mock('@/lib/workspace-activation-terminal-focus', () => ({
+  queueWorkspaceActivationTerminalFocus: vi.fn()
+}))
+vi.mock('sonner', () => ({ toast: { error: mocks.toastError } }))
+
+import { runBackgroundWorktreeCreation } from './worktree-creation-flow'
+
+beforeEach(() => {
+  vi.clearAllMocks()
+  mocks.store.activePendingCreationId = null
+  mocks.store.activeView = 'terminal'
+  mocks.store.pendingWorktreeCreations = {}
+  mocks.resolveExplicitRoute.mockReturnValue({
+    kind: 'resolved',
+    route: { executionHostId: 'ssh:requested', runtimeEnvironmentId: null }
+  })
+  mocks.store.createWorktree.mockResolvedValue({
+    worktree: { id: 'wt-shared', repoId: 'repo-1', hostId: 'ssh:requested' }
+  })
+})
+
+it('fails background startup closed when duplicate hosts make the bare id ambiguous', async () => {
+  mocks.store.activeView = 'tasks'
+  mocks.resolveExplicitRoute.mockReturnValue({ kind: 'ambiguous' })
+
+  runBackgroundWorktreeCreation({
+    repoId: 'repo-1',
+    name: 'remote-workspace',
+    setupDecision: 'inherit',
+    agent: 'codex',
+    pendingFirstAgentMessageRename: false,
+    note: '',
+    startupPlan: {
+      agent: 'codex',
+      launchCommand: 'codex',
+      expectedProcess: 'codex',
+      followupPrompt: null,
+      launchConfig: { agent: 'codex', command: 'codex' }
+    } as never,
+    quickPrompt: '',
+    quickTelemetry: null
+  })
+
+  await vi.waitFor(() => expect(mocks.toastError).toHaveBeenCalledTimes(1))
+  expect(mocks.ensureWorktreeHasInitialTerminal).not.toHaveBeenCalled()
+  expect(mocks.seedAgentTabState).not.toHaveBeenCalled()
+  expect(mocks.ensureAgentStartup).not.toHaveBeenCalled()
+})
+
+it('keeps remote host ownership through activation and note persistence', async () => {
+  runBackgroundWorktreeCreation({
+    repoId: 'repo-1',
+    name: 'remote-workspace',
+    setupDecision: 'inherit',
+    agent: null,
+    pendingFirstAgentMessageRename: false,
+    note: 'Remote note',
+    startupPlan: null,
+    quickPrompt: '',
+    quickTelemetry: null
+  })
+
+  await vi.waitFor(() =>
+    expect(mocks.activateAndRevealWorktree).toHaveBeenCalledWith('wt-shared', {
+      sidebarRevealBehavior: 'auto',
+      executionHostId: 'ssh:requested'
+    })
+  )
+  await vi.waitFor(() =>
+    expect(mocks.store.updateWorktreeMeta).toHaveBeenCalledWith(
+      'wt-shared',
+      { comment: 'Remote note' },
+      { executionHostId: 'ssh:requested' }
+    )
+  )
+})
diff --git a/src/renderer/src/lib/worktree-creation-flow.ts b/src/renderer/src/lib/worktree-creation-flow.ts
index b8748067479..94e7bb29116 100644
--- a/src/renderer/src/lib/worktree-creation-flow.ts
+++ b/src/renderer/src/lib/worktree-creation-flow.ts
@@ -1,6 +1,6 @@
 import { toast } from 'sonner'
 import { useAppStore } from '@/store'
-import { TUI_AGENT_CONFIG } from '../../../shared/tui-agent-config'
+import { translate } from '@/i18n/i18n'
 import {
   activateAndRevealWorktree,
   ensureWorktreeHasInitialTerminal,
@@ -27,6 +27,13 @@ import {
 import { createBrowserUuid } from '@/lib/browser-uuid'
 import { seedAgentTabStateAfterWorktreeCreate } from '@/lib/worktree-creation-agent-seeds'
 import { resolveBackendDraftStartup } from '@/lib/worktree-draft-startup-view-mode'
+import { findRepoForHost } from '@/store/slices/repo-host-identity'
+import { persistCreatedWorktreeNote } from '@/lib/worktree-creation-note'
+import { preflightWorktreeCreationAgentTrust } from '@/lib/worktree-creation-agent-trust'
+import {
+  canSeedCreatedWorktreeInBackground,
+  hasCreatedWorktreeTerminalHandoff
+} from '@/lib/worktree-creation-terminal-handoff'
 import {
   buildWorktreeCreationStartupOpt,
   getInitialWorktreeCreationPhase,
@@ -68,33 +75,6 @@ function revealPendingCreation(
   store.setSidebarOpen(true)
 }
 
-async function preflightAgentTrust(
-  request: WorktreeCreationRequest,
-  path: string,
-  connectionId?: string | null
-): Promise<void> {
-  // Why: trust-gated agents (cursor-agent, copilot) consume the bracketed paste
-  // as menu input on first launch. Pre-write the trust artifact before any
-  // terminal spawns. Best-effort — the worktree already exists, so a failure
-  // here must not strand it.
-  if (!request.agent || !window.api.agentTrust?.markTrusted) {
-    return
-  }
-  const preflight = TUI_AGENT_CONFIG[request.agent].preflightTrust
-  if (!preflight) {
-    return
-  }
-  try {
-    await window.api.agentTrust.markTrusted({
-      preset: preflight,
-      workspacePath: path,
-      ...(connectionId ? { connectionId } : {})
-    })
-  } catch {
-    // Best-effort: continue with launch.
-  }
-}
-
 async function executeWorktreeCreation(
   creationId: string,
   request: WorktreeCreationRequest
@@ -196,9 +176,13 @@ async function executeWorktreeCreation(
   const startupOpt = buildWorktreeCreationStartupOpt(preparedRequest, backendSpawned)
 
   if (worktree.path) {
+    const trustState = useAppStore.getState()
     const repoConnectionId =
-      useAppStore.getState().repos.find((repo) => repo.id === worktree.repoId)?.connectionId ?? null
-    await preflightAgentTrust(preparedRequest, worktree.path, repoConnectionId)
+      findRepoForHost(trustState.repos, worktree.repoId, {
+        hostId: worktree.hostId,
+        settings: trustState.settings
+      })?.connectionId ?? null
+    await preflightWorktreeCreationAgentTrust(preparedRequest, worktree.path, repoConnectionId)
   }
 
   // `createWorktree` already inserted the real worktree row. Leaving for an app
@@ -214,45 +198,63 @@ async function executeWorktreeCreation(
 
   let activation: ActivateAndRevealResult | false = false
   let primaryTabId: string | null
+  let terminalHandoffSafe = true
   if (shouldActivateOnCompletion) {
     activation = activateAndRevealWorktree(worktree.id, {
       sidebarRevealBehavior: 'auto',
+      ...(worktree.hostId ? { executionHostId: worktree.hostId } : {}),
       ...(result.setup ? { setup: result.setup } : {}),
       ...(result.defaultTabs ? { defaultTabs: result.defaultTabs } : {}),
       ...(startupOpt ? { startup: startupOpt } : {}),
       ...(preparedRequest.issueCommand ? { issueCommand: preparedRequest.issueCommand } : {}),
       ...(backendSpawned ? { backendStartupTerminalSpawned: true } : {})
     })
+    terminalHandoffSafe = activation !== false
     primaryTabId = activation === false ? null : activation.primaryTabId
   } else {
     // The user moved on. Seed the worktree's terminal + setup in the background
     // (setActiveTab only writes global focus for the active worktree, so this is
     // safe) without yanking them back to it.
-    primaryTabId = ensureWorktreeHasInitialTerminal(
-      useAppStore.getState(),
-      worktree.id,
-      startupOpt,
-      result.setup,
-      preparedRequest.issueCommand,
-      result.defaultTabs,
-      {
-        activateCreatedTabs: false,
-        ...(backendSpawned ? { backendStartupTerminalSpawned: true } : {})
+    terminalHandoffSafe = canSeedCreatedWorktreeInBackground(completionState, worktree)
+    if (!terminalHandoffSafe) {
+      primaryTabId = null
+      if (hasCreatedWorktreeTerminalHandoff(preparedRequest, result)) {
+        toast.error(
+          translate(
+            'auto.lib.worktreeCreationFlow.backgroundStartupOwnerAmbiguous',
+            'Workspace created, but automatic startup was skipped because its host is ambiguous.'
+          )
+        )
       }
-    )
+    } else {
+      primaryTabId = ensureWorktreeHasInitialTerminal(
+        completionState,
+        worktree.id,
+        startupOpt,
+        result.setup,
+        preparedRequest.issueCommand,
+        result.defaultTabs,
+        {
+          activateCreatedTabs: false,
+          ...(backendSpawned ? { backendStartupTerminalSpawned: true } : {})
+        }
+      )
+    }
   }
 
   // Why: clearing synchronously right after activation lets React commit the
   // panel→terminal swap in one frame — no two-row flicker, no empty-terminal flash.
   useAppStore.getState().removePendingWorktreeCreation(creationId, { cleanupVm: false })
-  seedAgentTabStateAfterWorktreeCreate({
-    request: preparedRequest,
-    worktreeId: worktree.id,
-    primaryTabId,
-    startupTerminalTabId: result.startupTerminal?.tabId,
-    backendSpawned
-  })
-  if (preparedRequest.startupPlan && !backendSpawned) {
+  if (terminalHandoffSafe) {
+    seedAgentTabStateAfterWorktreeCreate({
+      request: preparedRequest,
+      worktreeId: worktree.id,
+      primaryTabId,
+      startupTerminalTabId: result.startupTerminal?.tabId,
+      backendSpawned
+    })
+  }
+  if (terminalHandoffSafe && preparedRequest.startupPlan && !backendSpawned) {
     void ensureAgentStartupInTerminal({
       worktreeId: worktree.id,
       primaryTabId,
@@ -266,13 +268,7 @@ async function executeWorktreeCreation(
   // Why: awaiting the note IPC before the swap would add a visible round-trip to
   // the panel→terminal transition; it's cosmetic, so it runs last.
   if (preparedRequest.note) {
-    try {
-      await useAppStore.getState().updateWorktreeMeta(worktree.id, {
-        comment: preparedRequest.note
-      })
-    } catch {
-      console.error('Failed to update worktree meta after creation')
-    }
+    await persistCreatedWorktreeNote(worktree, preparedRequest.note)
   }
 }
 
diff --git a/src/renderer/src/lib/worktree-creation-note.ts b/src/renderer/src/lib/worktree-creation-note.ts
new file mode 100644
index 00000000000..9db439b1654
--- /dev/null
+++ b/src/renderer/src/lib/worktree-creation-note.ts
@@ -0,0 +1,19 @@
+import { useAppStore } from '@/store'
+import type { Worktree } from '../../../shared/types'
+
+export async function persistCreatedWorktreeNote(
+  worktree: Pick<Worktree, 'id' | 'hostId'>,
+  note: string
+): Promise<void> {
+  try {
+    await useAppStore
+      .getState()
+      .updateWorktreeMeta(
+        worktree.id,
+        { comment: note },
+        worktree.hostId ? { executionHostId: worktree.hostId } : undefined
+      )
+  } catch {
+    console.error('Failed to update worktree meta after creation')
+  }
+}
diff --git a/src/renderer/src/lib/worktree-creation-terminal-handoff.test.ts b/src/renderer/src/lib/worktree-creation-terminal-handoff.test.ts
new file mode 100644
index 00000000000..7951ddca621
--- /dev/null
+++ b/src/renderer/src/lib/worktree-creation-terminal-handoff.test.ts
@@ -0,0 +1,38 @@
+import { describe, expect, it } from 'vitest'
+import { canSeedCreatedWorktreeInBackground } from './worktree-creation-terminal-handoff'
+
+function stateWithOwners(owners: { id: string; repoId: string; hostId?: string }[]): never {
+  return {
+    repos: owners.map((owner) => ({
+      id: owner.repoId,
+      connectionId: owner.hostId?.startsWith('ssh:') ? owner.hostId.slice(4) : null,
+      executionHostId: owner.hostId
+    })),
+    worktreesByRepo: { repo: owners },
+    detectedWorktreesByRepo: {},
+    folderWorkspaces: [],
+    projectGroups: [],
+    runtimeEnvironments: [],
+    settings: {}
+  } as never
+}
+
+describe('created worktree background terminal handoff', () => {
+  it('fails closed when sibling hosts publish the same worktree id', () => {
+    const id = 'repo::/workspace'
+    const state = stateWithOwners([
+      { id, repoId: 'repo', hostId: 'ssh:first' },
+      { id, repoId: 'repo', hostId: 'ssh:second' }
+    ])
+
+    expect(canSeedCreatedWorktreeInBackground(state, { id, hostId: 'ssh:second' })).toBe(false)
+  })
+
+  it('allows a uniquely resolved host and preserves legacy hostless behavior', () => {
+    const id = 'repo::/workspace'
+    const state = stateWithOwners([{ id, repoId: 'repo', hostId: 'ssh:requested' }])
+
+    expect(canSeedCreatedWorktreeInBackground(state, { id, hostId: 'ssh:requested' })).toBe(true)
+    expect(canSeedCreatedWorktreeInBackground(state, { id })).toBe(true)
+  })
+})
diff --git a/src/renderer/src/lib/worktree-creation-terminal-handoff.ts b/src/renderer/src/lib/worktree-creation-terminal-handoff.ts
new file mode 100644
index 00000000000..1f51c80cd9c
--- /dev/null
+++ b/src/renderer/src/lib/worktree-creation-terminal-handoff.ts
@@ -0,0 +1,23 @@
+import type { CreateWorktreeResult, Worktree } from '../../../shared/types'
+import type { WorktreeCreationRequest } from './pending-worktree-creation'
+import { resolveExplicitWorktreeOperationRouteResult } from './worktree-operation-route'
+
+type RouteState = Parameters<typeof resolveExplicitWorktreeOperationRouteResult>[0]
+
+export function canSeedCreatedWorktreeInBackground(
+  state: RouteState,
+  worktree: Pick<Worktree, 'id' | 'hostId'>
+): boolean {
+  if (!worktree.hostId) {
+    return true
+  }
+  const resolution = resolveExplicitWorktreeOperationRouteResult(state, worktree.id)
+  return resolution.kind === 'resolved' && resolution.route.executionHostId === worktree.hostId
+}
+
+export function hasCreatedWorktreeTerminalHandoff(
+  request: WorktreeCreationRequest,
+  result: CreateWorktreeResult
+): boolean {
+  return Boolean(request.startupPlan || result.setup || request.issueCommand || result.defaultTabs)
+}