diff --git a/apps/desktop/src/app/desktop-controller.tsx b/apps/desktop/src/app/desktop-controller.tsx
index cb7b10f655b..2ff2ff176e7 100644
--- a/apps/desktop/src/app/desktop-controller.tsx
+++ b/apps/desktop/src/app/desktop-controller.tsx
@@ -812,6 +812,7 @@ export function DesktopController() {
     branchCurrentSession: branchInNewChat,
     busyRef,
     createBackendSessionForSend,
+    getRouteToken,
     handleSkinCommand,
     openMemoryGraph: openStarmap,
     refreshSessions,
diff --git a/apps/desktop/src/app/session/hooks/use-prompt-actions/index.test.tsx b/apps/desktop/src/app/session/hooks/use-prompt-actions/index.test.tsx
index 045a4e7975d..5f028876a8e 100644
--- a/apps/desktop/src/app/session/hooks/use-prompt-actions/index.test.tsx
+++ b/apps/desktop/src/app/session/hooks/use-prompt-actions/index.test.tsx
@@ -51,7 +51,9 @@ interface HarnessHandle {
 }
 
 function Harness({
+  activeSessionIdRef: activeSessionIdRefProp,
   busyRef,
+  getRouteToken,
   onReady,
   onSeedState,
   openMemoryGraph,
@@ -59,11 +61,14 @@ function Harness({
   requestGateway,
   resumeStoredSession,
   seedMessages,
+  selectedStoredSessionIdRef: selectedStoredSessionIdRefProp,
   storedSessionId,
   activeSessionId,
   createBackendSessionForSend
 }: {
+  activeSessionIdRef?: MutableRefObject<string | null>
   busyRef?: MutableRefObject<boolean>
+  getRouteToken?: () => string
   onReady: (handle: HarnessHandle) => void
   onSeedState?: (state: Record<string, unknown>) => void
   openMemoryGraph?: () => void
@@ -71,15 +76,16 @@ function Harness({
   requestGateway: <T>(method: string, params?: Record<string, unknown>) => Promise<T>
   resumeStoredSession?: (storedSessionId: string) => Promise<void> | void
   seedMessages?: unknown[]
+  selectedStoredSessionIdRef?: MutableRefObject<string | null>
   storedSessionId?: null | string
   activeSessionId?: null | string
   createBackendSessionForSend?: () => Promise<null | string>
 }) {
-  const activeSessionIdRef: MutableRefObject<string | null> = {
+  const activeSessionIdRef: MutableRefObject<string | null> = activeSessionIdRefProp ?? {
     current: activeSessionId === undefined ? RUNTIME_SESSION_ID : activeSessionId
   }
 
-  const selectedStoredSessionIdRef: MutableRefObject<string | null> = {
+  const selectedStoredSessionIdRef: MutableRefObject<string | null> = selectedStoredSessionIdRefProp ?? {
     current: storedSessionId === undefined ? RUNTIME_SESSION_ID : storedSessionId
   }
 
@@ -98,6 +104,7 @@ function Harness({
     branchCurrentSession: async () => true,
     busyRef: localBusyRef,
     createBackendSessionForSend: createBackendSessionForSend ?? (async () => RUNTIME_SESSION_ID),
+    getRouteToken: getRouteToken ?? (() => 'token'),
     handleSkinCommand: () => '',
     openMemoryGraph: openMemoryGraph ?? (() => undefined),
     refreshSessions,
@@ -1239,7 +1246,7 @@ describe('usePromptActions sleep/wake session recovery', () => {
 
     expect(ok).toBe(true)
     expect(calls.map(c => c.method)).toEqual(['prompt.submit', 'session.resume', 'prompt.submit'])
-    expect(calls[1]?.params).toEqual({ session_id: STORED_SESSION_ID })
+    expect(calls[1]?.params).toEqual({ session_id: STORED_SESSION_ID, source: 'desktop' })
     expect(calls[2]?.params).toEqual({
       session_id: RECOVERED_SESSION_ID,
       text: 'message during starved loop'
@@ -1316,6 +1323,125 @@ describe('usePromptActions sleep/wake session recovery', () => {
   })
 })
 
+describe('usePromptActions submit session-context isolation (#54527)', () => {
+  const STORED_SESSION_A = 'stored-project-a'
+  const STORED_SESSION_B = 'stored-project-b'
+  const RUNTIME_SESSION_B = 'rt-session-b-wrong'
+
+  afterEach(() => {
+    cleanup()
+    vi.restoreAllMocks()
+  })
+
+  it('aborts submit when the user switches sessions during session.resume (no misroute)', async () => {
+    // Exact #54527 failure: user submits in Session A while its runtime binding
+    // is gone; before resume returns they switch to Session B. Without a pinned
+    // context the resumed runtime id belongs to B and A's text lands in the
+    // wrong chat — permanently lost from A.
+    let releaseResume: () => void = () => {}
+    const calls: { method: string; params?: Record<string, unknown> }[] = []
+
+    const selectedStoredSessionIdRef: MutableRefObject<string | null> = { current: STORED_SESSION_A }
+    const activeSessionIdRef: MutableRefObject<string | null> = { current: null }
+
+    const requestGateway = vi.fn(async (method: string, params?: Record<string, unknown>) => {
+      calls.push({ method, params })
+
+      if (method === 'session.resume') {
+        await new Promise<void>(resolve => {
+          releaseResume = resolve
+        })
+
+        // Simulate the user switching to Session B while resume is in flight.
+        selectedStoredSessionIdRef.current = STORED_SESSION_B
+        activeSessionIdRef.current = RUNTIME_SESSION_B
+
+        return { session_id: RUNTIME_SESSION_B } as never
+      }
+
+      return {} as never
+    })
+
+    let handle: HarnessHandle | null = null
+    render(
+      <Harness
+        activeSessionId={null}
+        activeSessionIdRef={activeSessionIdRef}
+        onReady={h => (handle = h)}
+        refreshSessions={async () => undefined}
+        requestGateway={requestGateway}
+        selectedStoredSessionIdRef={selectedStoredSessionIdRef}
+        storedSessionId={STORED_SESSION_A}
+      />
+    )
+    await waitFor(() => expect(handle).not.toBeNull())
+
+    const submitting = handle!.submitText('carefully composed prompt for project A')
+    await waitFor(() => expect(calls.some(c => c.method === 'session.resume')).toBe(true))
+    releaseResume()
+
+    expect(await submitting).toBe(false)
+    expect(calls.some(c => c.method === 'prompt.submit')).toBe(false)
+    expect(calls.find(c => c.method === 'session.resume')?.params).toEqual({
+      session_id: STORED_SESSION_A
+    })
+  })
+
+  it('aborts recovery submit when the user switches sessions during timeout resume', async () => {
+    const calls: { method: string; params?: Record<string, unknown> }[] = []
+    let submitAttempts = 0
+    let releaseResume: () => void = () => {}
+
+    const selectedStoredSessionIdRef: MutableRefObject<string | null> = { current: STORED_SESSION_A }
+
+    const requestGateway = vi.fn(async (method: string, params?: Record<string, unknown>) => {
+      calls.push({ method, params })
+
+      if (method === 'prompt.submit') {
+        submitAttempts += 1
+
+        if (submitAttempts === 1) {
+          throw new Error('request timed out: prompt.submit')
+        }
+      }
+
+      if (method === 'session.resume') {
+        await new Promise<void>(resolve => {
+          releaseResume = resolve
+        })
+        selectedStoredSessionIdRef.current = STORED_SESSION_B
+
+        return { session_id: RUNTIME_SESSION_B } as never
+      }
+
+      return {} as never
+    })
+
+    let handle: HarnessHandle | null = null
+    render(
+      <Harness
+        onReady={h => (handle = h)}
+        refreshSessions={async () => undefined}
+        requestGateway={requestGateway}
+        selectedStoredSessionIdRef={selectedStoredSessionIdRef}
+        storedSessionId={STORED_SESSION_A}
+      />
+    )
+    await waitFor(() => expect(handle).not.toBeNull())
+
+    const submitting = handle!.submitText('message that must not land in session B')
+    await waitFor(() => expect(calls.some(c => c.method === 'session.resume')).toBe(true))
+    releaseResume()
+
+    expect(await submitting).toBe(false)
+    expect(submitAttempts).toBe(1)
+    expect(calls.filter(c => c.method === 'prompt.submit')).toHaveLength(1)
+    expect(calls.find(c => c.method === 'session.resume')?.params).toMatchObject({
+      session_id: STORED_SESSION_A
+    })
+  })
+})
+
 describe('usePromptActions eager attachment upload (drop-time)', () => {
   afterEach(() => {
     cleanup()
diff --git a/apps/desktop/src/app/session/hooks/use-prompt-actions/index.ts b/apps/desktop/src/app/session/hooks/use-prompt-actions/index.ts
index 8ebe8889d16..51a3689ae4e 100644
--- a/apps/desktop/src/app/session/hooks/use-prompt-actions/index.ts
+++ b/apps/desktop/src/app/session/hooks/use-prompt-actions/index.ts
@@ -158,6 +158,7 @@ interface PromptActionsOptions {
   busyRef: MutableRefObject<boolean>
   branchCurrentSession: () => Promise<boolean>
   createBackendSessionForSend: (preview?: string | null) => Promise<string | null>
+  getRouteToken: () => string
   handleSkinCommand: (arg: string) => string
   openMemoryGraph: () => void
   refreshSessions: () => Promise<void>
@@ -186,6 +187,7 @@ export function usePromptActions({
   busyRef,
   branchCurrentSession,
   createBackendSessionForSend,
+  getRouteToken,
   handleSkinCommand,
   openMemoryGraph,
   refreshSessions,
@@ -354,6 +356,7 @@ export function usePromptActions({
     busyRef,
     copy,
     createBackendSessionForSend,
+    getRouteToken,
     requestGateway,
     selectedStoredSessionIdRef,
     syncAttachmentsForSubmit,
diff --git a/apps/desktop/src/app/session/hooks/use-prompt-actions/submit.ts b/apps/desktop/src/app/session/hooks/use-prompt-actions/submit.ts
index 6b2049f892b..5dd01fc6d6d 100644
--- a/apps/desktop/src/app/session/hooks/use-prompt-actions/submit.ts
+++ b/apps/desktop/src/app/session/hooks/use-prompt-actions/submit.ts
@@ -35,6 +35,7 @@ interface SubmitPromptDeps {
   busyRef: MutableRefObject<boolean>
   copy: Translations['desktop']
   createBackendSessionForSend: (preview?: string | null) => Promise<string | null>
+  getRouteToken: () => string
   requestGateway: GatewayRequest
   selectedStoredSessionIdRef: MutableRefObject<string | null>
   syncAttachmentsForSubmit: (
@@ -57,6 +58,7 @@ export function useSubmitPrompt(deps: SubmitPromptDeps) {
     busyRef,
     copy,
     createBackendSessionForSend,
+    getRouteToken,
     requestGateway,
     selectedStoredSessionIdRef,
     syncAttachmentsForSubmit,
@@ -113,9 +115,20 @@ export function useSubmitPrompt(deps: SubmitPromptDeps) {
         return false
       }
 
+      // Pin the session context for the whole async submit pipeline. Without
+      // this, a fast session switch during session.resume / file.attach can
+      // redirect the user's text into a different chat (#54527).
+      const startingActiveSessionId = activeSessionIdRef.current
+      const startingStoredSessionId = selectedStoredSessionIdRef.current
+      const startingRouteToken = getRouteToken()
+
+      const sessionContextDrifted = (): boolean =>
+        selectedStoredSessionIdRef.current !== startingStoredSessionId ||
+        getRouteToken() !== startingRouteToken
+
       // One submit in flight per session — drop any concurrent re-fire so a
       // stalled turn can't stack the same prompt into multiple real turns.
-      const submitLockKey = selectedStoredSessionIdRef.current || activeSessionId || '__pending_new__'
+      const submitLockKey = startingStoredSessionId || startingActiveSessionId || '__pending_new__'
 
       if (_submitInFlight.has(submitLockKey)) {
         return false
@@ -166,7 +179,7 @@ export function useSubmitPrompt(deps: SubmitPromptDeps) {
             // (what made drained-after-interrupt sends go silent).
             interrupted: false
           }),
-          selectedStoredSessionIdRef.current
+          startingStoredSessionId
         )
 
       // After sync rewrites refs, refresh the optimistic message in place so the
@@ -178,7 +191,7 @@ export function useSubmitPrompt(deps: SubmitPromptDeps) {
             ...state,
             messages: state.messages.map(message => (message.id === optimisticId ? buildUserMessage() : message))
           }),
-          selectedStoredSessionIdRef.current
+          startingStoredSessionId
         )
 
       const dropOptimistic = (sid: null | string) => {
@@ -197,10 +210,17 @@ export function useSubmitPrompt(deps: SubmitPromptDeps) {
             awaitingResponse: false,
             pendingBranchGroup: null
           }),
-          selectedStoredSessionIdRef.current
+          startingStoredSessionId
         )
       }
 
+      const abortForSessionSwitch = (optimisticSessionId: null | string): false => {
+        dropOptimistic(optimisticSessionId)
+        releaseBusy()
+
+        return false
+      }
+
       setMutableRef(busyRef, true)
       setBusy(true)
       setAwaitingResponse(true)
@@ -214,7 +234,7 @@ export function useSubmitPrompt(deps: SubmitPromptDeps) {
         setMessages(current => [...current, buildUserMessage()])
       }
 
-      if (!sessionId && selectedStoredSessionIdRef.current) {
+      if (!sessionId && startingStoredSessionId) {
         // A stored session is SELECTED but its runtime binding is gone (the
         // live session was orphan-reaped, or a timeout/reconnect cleared
         // activeSessionId). Continuing the selected conversation must mean
@@ -224,9 +244,13 @@ export function useSubmitPrompt(deps: SubmitPromptDeps) {
         // new-chat draft).
         try {
           const resumed = await requestGateway<{ session_id: string }>('session.resume', {
-            session_id: selectedStoredSessionIdRef.current
+            session_id: startingStoredSessionId
           })
 
+          if (sessionContextDrifted()) {
+            return abortForSessionSwitch(sessionId)
+          }
+
           if (resumed?.session_id) {
             sessionId = resumed.session_id
             activeSessionIdRef.current = sessionId
@@ -237,6 +261,10 @@ export function useSubmitPrompt(deps: SubmitPromptDeps) {
           // the user's message.
         }
 
+        if (sessionContextDrifted()) {
+          return abortForSessionSwitch(sessionId)
+        }
+
         if (sessionId) {
           seedOptimistic(sessionId)
         }
@@ -253,6 +281,10 @@ export function useSubmitPrompt(deps: SubmitPromptDeps) {
           return false
         }
 
+        if (sessionContextDrifted()) {
+          return abortForSessionSwitch(sessionId)
+        }
+
         if (!sessionId) {
           dropOptimistic(null)
           releaseBusy()
@@ -269,6 +301,10 @@ export function useSubmitPrompt(deps: SubmitPromptDeps) {
           updateComposerAttachments: usingComposerAttachments
         })
 
+        if (sessionContextDrifted()) {
+          return abortForSessionSwitch(sessionId)
+        }
+
         // Rewrite the optimistic message + prompt text with the synced refs so
         // the gateway receives @file: paths that resolve in its workspace.
         // (Images keep their inline base64 preview — see optimisticAttachmentRef.)
@@ -288,7 +324,7 @@ export function useSubmitPrompt(deps: SubmitPromptDeps) {
         } catch (firstErr) {
           if (
             (isSessionNotFoundError(firstErr) || isGatewayTimeoutError(firstErr)) &&
-            selectedStoredSessionIdRef.current
+            startingStoredSessionId
           ) {
             // Re-register the session in the gateway and get a fresh live ID.
             // Timeouts recover the same way as "session not found": a starved
@@ -296,10 +332,14 @@ export function useSubmitPrompt(deps: SubmitPromptDeps) {
             // the stored session is fine — resume + retry instead of erroring
             // out and losing the session binding.
             const resumed = await requestGateway<{ session_id: string }>('session.resume', {
-              session_id: selectedStoredSessionIdRef.current,
+              session_id: startingStoredSessionId,
               source: 'desktop'
             })
 
+            if (sessionContextDrifted()) {
+              return abortForSessionSwitch(sessionId)
+            }
+
             const recoveredId = resumed?.session_id
 
             if (recoveredId) {
@@ -375,6 +415,7 @@ export function useSubmitPrompt(deps: SubmitPromptDeps) {
       busyRef,
       copy,
       createBackendSessionForSend,
+      getRouteToken,
       requestGateway,
       selectedStoredSessionIdRef,
       syncAttachmentsForSubmit,