diff --git a/apps/desktop/src/components/prompt-overlays.test.tsx b/apps/desktop/src/components/prompt-overlays.test.tsx
new file mode 100644
index 000000000000..7b8cb2148f5e
--- /dev/null
+++ b/apps/desktop/src/components/prompt-overlays.test.tsx
@@ -0,0 +1,67 @@
+import { cleanup, fireEvent, render, screen, waitFor } from '@testing-library/react'
+import { afterEach, describe, expect, it, vi } from 'vitest'
+
+import { I18nProvider } from '@/i18n'
+import { $gateway } from '@/store/gateway'
+import { notifyError } from '@/store/notifications'
+import { $secretRequest, $sudoRequest, clearAllPrompts, setSecretRequest, setSudoRequest } from '@/store/prompts'
+import { $activeSessionId } from '@/store/session'
+
+import { PromptOverlays } from './prompt-overlays'
+
+vi.mock('@/lib/haptics', () => ({ triggerHaptic: vi.fn() }))
+vi.mock('@/store/notifications', () => ({ notifyError: vi.fn() }))
+
+function renderPrompts() {
+  render(
+    <I18nProvider configClient={null}>
+      <PromptOverlays />
+    </I18nProvider>
+  )
+}
+
+afterEach(() => {
+  cleanup()
+  clearAllPrompts()
+  $activeSessionId.set(null)
+  $gateway.set(null)
+  vi.clearAllMocks()
+})
+
+describe('PromptOverlays', () => {
+  it('dismisses a stale sudo dialog when the gateway no longer has the password request', async () => {
+    const request = vi.fn().mockRejectedValue(new Error('no pending password request'))
+
+    $activeSessionId.set('s1')
+    $gateway.set({ request } as never)
+    setSudoRequest({ requestId: 'sudo-1', sessionId: 's1' })
+
+    renderPrompts()
+
+    expect(screen.getByText('Administrator password')).toBeTruthy()
+
+    fireEvent.click(screen.getByRole('button', { name: 'Cancel' }))
+
+    await waitFor(() => expect($sudoRequest.get()).toBeNull())
+    expect(request).toHaveBeenCalledWith('sudo.respond', { password: '', request_id: 'sudo-1' })
+    expect(notifyError).not.toHaveBeenCalled()
+  })
+
+  it('dismisses a stale secret dialog when the gateway no longer has the value request', async () => {
+    const request = vi.fn().mockRejectedValue(new Error('no pending value request'))
+
+    $activeSessionId.set('s1')
+    $gateway.set({ request } as never)
+    setSecretRequest({ envVar: 'TEST_SECRET', prompt: 'Paste a secret', requestId: 'secret-1', sessionId: 's1' })
+
+    renderPrompts()
+
+    expect(screen.getByText('TEST_SECRET')).toBeTruthy()
+
+    fireEvent.click(screen.getByRole('button', { name: 'Cancel' }))
+
+    await waitFor(() => expect($secretRequest.get()).toBeNull())
+    expect(request).toHaveBeenCalledWith('secret.respond', { request_id: 'secret-1', value: '' })
+    expect(notifyError).not.toHaveBeenCalled()
+  })
+})
diff --git a/apps/desktop/src/components/prompt-overlays.tsx b/apps/desktop/src/components/prompt-overlays.tsx
index a43303e1ced3..cf56d62e85ad 100644
--- a/apps/desktop/src/components/prompt-overlays.tsx
+++ b/apps/desktop/src/components/prompt-overlays.tsx
@@ -15,6 +15,7 @@ import {
 } from '@/components/ui/dialog'
 import { Input } from '@/components/ui/input'
 import { useI18n } from '@/i18n'
+import { isMissingPendingPromptRequest } from '@/lib/gateway-rpc'
 import { triggerHaptic } from '@/lib/haptics'
 import { KeyRound, Loader2, Lock } from '@/lib/icons'
 import { $gateway } from '@/store/gateway'
@@ -69,6 +70,12 @@ function SudoDialog() {
         triggerHaptic('submit')
         clearSudoRequest(request.sessionId, request.requestId)
       } catch (error) {
+        if (isMissingPendingPromptRequest(error, 'password')) {
+          clearSudoRequest(request.sessionId, request.requestId)
+
+          return
+        }
+
         notifyError(error, copy.sudoSendFailed)
         setSubmitting(false)
       }
@@ -165,6 +172,12 @@ function SecretDialog() {
         triggerHaptic('submit')
         clearSecretRequest(request.sessionId, request.requestId)
       } catch (error) {
+        if (isMissingPendingPromptRequest(error, 'value')) {
+          clearSecretRequest(request.sessionId, request.requestId)
+
+          return
+        }
+
         notifyError(error, copy.secretSendFailed)
         setSubmitting(false)
       }
diff --git a/apps/desktop/src/lib/gateway-rpc.test.ts b/apps/desktop/src/lib/gateway-rpc.test.ts
index 6da30b87b765..6c84c12ecaa8 100644
--- a/apps/desktop/src/lib/gateway-rpc.test.ts
+++ b/apps/desktop/src/lib/gateway-rpc.test.ts
@@ -1,6 +1,6 @@
 import { describe, expect, it } from 'vitest'
 
-import { isMissingRpcMethod } from './gateway-rpc'
+import { isMissingPendingPromptRequest, isMissingRpcMethod } from './gateway-rpc'
 
 describe('isMissingRpcMethod', () => {
   it('detects JSON-RPC method-not-found errors', () => {
@@ -14,3 +14,15 @@ describe('isMissingRpcMethod', () => {
     expect(isMissingRpcMethod(new Error('no such project'))).toBe(false)
   })
 })
+
+describe('isMissingPendingPromptRequest', () => {
+  it('detects stale prompt response errors from the gateway', () => {
+    expect(isMissingPendingPromptRequest(new Error('no pending password request'), 'password')).toBe(true)
+    expect(isMissingPendingPromptRequest(new Error('RPC failed: no pending value request'), 'value')).toBe(true)
+  })
+
+  it('ignores unrelated gateway failures', () => {
+    expect(isMissingPendingPromptRequest(new Error('gateway not connected'), 'password')).toBe(false)
+    expect(isMissingPendingPromptRequest(new Error('no pending value request'), 'password')).toBe(false)
+  })
+})
diff --git a/apps/desktop/src/lib/gateway-rpc.ts b/apps/desktop/src/lib/gateway-rpc.ts
index a209aefbd001..6cf298402f32 100644
--- a/apps/desktop/src/lib/gateway-rpc.ts
+++ b/apps/desktop/src/lib/gateway-rpc.ts
@@ -4,3 +4,10 @@ export function isMissingRpcMethod(error: unknown): boolean {
 
   return /method not found|-32601|unknown method|no such method/i.test(message)
 }
+
+/** True when a prompt response raced a backend-side timeout / completion. */
+export function isMissingPendingPromptRequest(error: unknown, key: string): boolean {
+  const message = error instanceof Error ? error.message : String(error)
+
+  return message.toLowerCase().includes(`no pending ${key.toLowerCase()} request`)
+}