diff --git a/src/renderer/src/components/terminal-pane/remote-runtime-pty-transport.test.ts b/src/renderer/src/components/terminal-pane/remote-runtime-pty-transport.test.ts
index 78c7c43548f..4a9dfbbea00 100644
--- a/src/renderer/src/components/terminal-pane/remote-runtime-pty-transport.test.ts
+++ b/src/renderer/src/components/terminal-pane/remote-runtime-pty-transport.test.ts
@@ -490,39 +490,51 @@ describe('createRemoteRuntimePtyTransport', () => {
     const draft = 'QA regular reconnect draft - keep this unsent'
     emitOutput(initialStreamId, draft)
 
-    runtimeCall.mockImplementation(async (args: { method: string }) =>
-      args.method === 'session.tabs.list'
-        ? {
-            ok: true,
-            result: {
-              worktree: 'wt-1',
-              publicationEpoch: 'epoch-1',
-              snapshotVersion: 2,
-              activeGroupId: null,
-              activeTabId: 'tab-1::pane:1',
-              activeTabType: 'terminal',
-              tabs: [
-                {
-                  type: 'terminal',
-                  id: 'tab-1::pane:1',
-                  parentTabId: 'tab-1',
-                  leafId: 'pane:1',
-                  title: 'Claude Code',
-                  isActive: true,
-                  status: 'ready',
-                  terminal: 'terminal-reconnected'
-                }
-              ]
-            }
+    let hostListCalls = 0
+    runtimeCall.mockImplementation(async (args: { method: string }) => {
+      if (args.method === 'session.tabs.list') {
+        hostListCalls += 1
+        const terminal =
+          hostListCalls === 1
+            ? 'terminal-stale'
+            : hostListCalls === 2
+              ? null
+              : 'terminal-reconnected'
+        return {
+          ok: true,
+          result: {
+            worktree: 'wt-1',
+            publicationEpoch: 'epoch-1',
+            snapshotVersion: hostListCalls + 1,
+            activeGroupId: null,
+            activeTabId: 'tab-1::pane:1',
+            activeTabType: 'terminal',
+            tabs: [
+              {
+                type: 'terminal',
+                id: 'tab-1::pane:1',
+                parentTabId: 'tab-1',
+                leafId: 'pane:1',
+                title: 'Claude Code',
+                isActive: true,
+                status: terminal ? 'ready' : 'pending-handle',
+                terminal
+              }
+            ]
           }
-        : { ok: true, result: {} }
-    )
+        }
+      }
+      return { ok: true, result: {} }
+    })
 
     subscriptionCallbacks?.onResponse({
       ok: true,
       result: { type: 'error', streamId: initialStreamId, message: 'terminal_handle_stale' }
     })
 
+    await vi.waitFor(() => expect(hostListCalls).toBeGreaterThanOrEqual(1))
+    expect(latestSubscribePayload()).toMatchObject({ terminal: 'terminal-stale' })
+    expect(onPtyExit).not.toHaveBeenCalled()
     await vi.waitFor(() =>
       expect(latestSubscribePayload()).toMatchObject({ terminal: 'terminal-reconnected' })
     )
@@ -536,6 +548,17 @@ describe('createRemoteRuntimePtyTransport', () => {
     expect(transport.getPtyId()).toBe('remote:env-1@@terminal-reconnected')
     expect(transport.isConnected()).toBe(true)
     expect(renderedScreen.at(-1)).toBe(draft)
+    expect(hostListCalls).toBe(3)
+    const subscribedTerminals = subscriptionSendBinary.mock.calls
+      .map((call) => decodeTerminalStreamFrame(call[0]))
+      .flatMap((frame) => {
+        if (frame?.opcode !== TerminalStreamOpcode.Subscribe) {
+          return []
+        }
+        const payload = decodeTerminalStreamJson<{ terminal: string }>(frame.payload)
+        return payload ? [payload.terminal] : []
+      })
+    expect(subscribedTerminals).toEqual(['terminal-stale', 'terminal-reconnected'])
   })
 
   it('still retires the regular TUI surface after an explicit terminal exit', async () => {
diff --git a/src/renderer/src/components/terminal-pane/remote-runtime-pty-transport.ts b/src/renderer/src/components/terminal-pane/remote-runtime-pty-transport.ts
index 829c30106a7..dc3aa31e583 100644
--- a/src/renderer/src/components/terminal-pane/remote-runtime-pty-transport.ts
+++ b/src/renderer/src/components/terminal-pane/remote-runtime-pty-transport.ts
@@ -40,6 +40,7 @@ import { isWebTerminalSurfaceTabId, toHostSessionTabId } from '@/runtime/web-ter
 const REMOTE_TERMINAL_INPUT_FLUSH_MS = 8
 const REMOTE_TERMINAL_VIEWPORT_FLUSH_MS = 33
 const HOST_SESSION_ATTACH_POLL_MS = 150
+const HOST_SESSION_REPLACEMENT_POLL_MAX_MS = 1_000
 const HOST_SESSION_ATTACH_TIMEOUT_MS = 15_000
 
 function isRemoteTerminalStaleMessage(message: string): boolean {
@@ -94,6 +95,7 @@ export function createRemoteRuntimePtyTransport(
   let storedCallbacks: Parameters<PtyTransport['connect']>[0]['callbacks'] = {}
   let resubscribing = false
   let resubscribeRequested = false
+  let resubscribeRequiresReplacement = false
   let subscriptionGeneration = 0
   let pendingViewportClaim = false
   let pendingClaimInput = ''
@@ -212,6 +214,39 @@ export function createRemoteRuntimePtyTransport(
     return findReadyHostSessionHandle(listed, hostTabId)
   }
 
+  async function waitForReplacementHostSessionHandle(
+    hostTabId: string,
+    previousHandle: string
+  ): Promise<string | null> {
+    if (!worktreeId) {
+      return null
+    }
+    const worktree = toRuntimeWorktreeSelector(worktreeId)
+    const startedAt = Date.now()
+    let pollMs = HOST_SESSION_ATTACH_POLL_MS
+    while (!destroyed && connected && handle === previousHandle) {
+      const listed = await callRuntime<RuntimeMobileSessionTabsResult>('session.tabs.list', {
+        worktree
+      })
+      const nextHandle = findReadyHostSessionHandle(listed, hostTabId)
+      if (nextHandle && nextHandle !== previousHandle) {
+        return nextHandle
+      }
+      if (!hasHostSessionTerminalSurface(listed, hostTabId)) {
+        return null
+      }
+      const remainingMs = HOST_SESSION_ATTACH_TIMEOUT_MS - (Date.now() - startedAt)
+      if (remainingMs <= 0) {
+        return null
+      }
+      // Why: a stale response can precede publication of its replacement.
+      // Bounded backoff avoids retrying the known-stale handle in a hot loop.
+      await new Promise((resolve) => setTimeout(resolve, Math.min(pollMs, remainingMs)))
+      pollMs = Math.min(pollMs * 2, HOST_SESSION_REPLACEMENT_POLL_MAX_MS)
+    }
+    return null
+  }
+
   async function attachHostSessionMirror(
     options: Parameters<PtyTransport['connect']>[0]
   ): Promise<PtyConnectResult | undefined> {
@@ -429,7 +464,7 @@ export function createRemoteRuntimePtyTransport(
         // Why: reconnect can re-mint a mirrored pane's handle while its host tab
         // remains alive. Keep xterm/composer state mounted while we re-resolve it.
         closeMultiplexedStream()
-        scheduleResubscribeAfterTransportClose()
+        scheduleResubscribeAfterTransportClose(true)
       } else {
         retireRemoteTerminalId()
       }
@@ -448,9 +483,15 @@ export function createRemoteRuntimePtyTransport(
   // handle (reconnect, epoch or PTY change). Re-derive it from the current
   // session snapshot instead of resubscribing the stale closure value, which
   // would mirror (and type into) whatever PTY now sits behind it (#7718).
-  async function resubscribeAfterTransportClose(previousHandle: string): Promise<void> {
+  async function resubscribeAfterTransportClose(
+    previousHandle: string,
+    requireReplacement: boolean
+  ): Promise<void> {
     if (tabId && isWebTerminalSurfaceTabId(tabId)) {
-      const nextHandle = await listHostSessionHandle(toHostSessionTabId(tabId))
+      const hostTabId = toHostSessionTabId(tabId)
+      const nextHandle = requireReplacement
+        ? await waitForReplacementHostSessionHandle(hostTabId, previousHandle)
+        : await listHostSessionHandle(hostTabId)
       if (destroyed || !connected || handle !== previousHandle) {
         return
       }
@@ -469,17 +510,18 @@ export function createRemoteRuntimePtyTransport(
     await subscribeToHandle()
   }
 
-  function scheduleResubscribeAfterTransportClose(): void {
+  function scheduleResubscribeAfterTransportClose(requireReplacement = false): void {
     if (destroyed || !connected || !handle) {
       return
     }
     if (resubscribing) {
       resubscribeRequested = true
+      resubscribeRequiresReplacement ||= requireReplacement
       return
     }
     resubscribing = true
     const resubscribeHandle = handle
-    void resubscribeAfterTransportClose(resubscribeHandle)
+    void resubscribeAfterTransportClose(resubscribeHandle, requireReplacement)
       .catch((error) => {
         if (!destroyed && connected && handle) {
           clearPendingViewportClaim()
@@ -490,7 +532,9 @@ export function createRemoteRuntimePtyTransport(
         resubscribing = false
         if (resubscribeRequested) {
           resubscribeRequested = false
-          scheduleResubscribeAfterTransportClose()
+          const pendingRequiresReplacement = resubscribeRequiresReplacement
+          resubscribeRequiresReplacement = false
+          scheduleResubscribeAfterTransportClose(pendingRequiresReplacement)
         }
       })
   }