diff --git a/src/main/hosted-sandbox/hosted-agent-auto-resume.ts b/src/main/hosted-sandbox/hosted-agent-auto-resume.ts
index 2c1a1fd8e47..fced9e50cd1 100644
--- a/src/main/hosted-sandbox/hosted-agent-auto-resume.ts
+++ b/src/main/hosted-sandbox/hosted-agent-auto-resume.ts
@@ -24,13 +24,51 @@ const ContinueAnswer = z.looseObject({
   skipped: z.array(z.unknown()).optional()
 })
 
+/** `recordedAt` is the host's clock and `drainStartedAt` this machine's: tolerate skew between
+ *  them so an offer the drain just recorded is not mistaken for an older one. */
+export const CLOCK_SKEW_TOLERANCE_MS = 2 * 60_000
+/** A host too slow to list its offers before a restart is treated as unable to (falls back to time). */
+const OFFER_SNAPSHOT_TIMEOUT_MS = 5_000
+
 function hasCode(error: unknown, code: string): boolean {
   return typeof error === 'object' && error !== null && 'code' in error && error.code === code
 }
 
+/** Offer ids the host already holds before a drain; offers in it were left for the user. Null when
+ *  the host cannot answer (an unresponsive host is often why it is being restarted). */
+export async function listRestartOfferIds(call: RuntimeCall): Promise<ReadonlySet<string> | null> {
+  try {
+    let timer: ReturnType<typeof setTimeout> | undefined
+    const listed = await Promise.race([
+      call('agentSession.restartResumable'),
+      new Promise<null>((resolve) => {
+        timer = setTimeout(() => resolve(null), OFFER_SNAPSHOT_TIMEOUT_MS)
+      })
+    ]).finally(() => clearTimeout(timer))
+    const list = OfferList.safeParse(listed)
+    if (!list.success) {
+      return null
+    }
+    return new Set(
+      list.data.sessions.flatMap((row) => {
+        const offer = Offer.safeParse(row)
+        return offer.success ? [offer.data.sessionId] : []
+      })
+    )
+  } catch {
+    return null
+  }
+}
+
+/**
+ * Continues the offers this drain recorded. With a pre-drain snapshot of the host's offers, "recorded
+ * by this drain" is set membership (no clock comparison); without one it falls back to the host
+ * timestamp against this machine's drain start, allowing for clock skew.
+ */
 export async function autoResumeAgentsAfterRollover(
   call: RuntimeCall,
-  drainStartedAt: number
+  drainStartedAt: number,
+  offersBeforeDrain: ReadonlySet<string> | null = null
 ): Promise<HostedAgentAutoResumeOutcome> {
   let listed: unknown
   try {
@@ -47,7 +85,13 @@ export async function autoResumeAgentsAfterRollover(
   }
   const ids = list.data.sessions.flatMap((row) => {
     const offer = Offer.safeParse(row)
-    return offer.success && offer.data.recordedAt >= drainStartedAt ? [offer.data.sessionId] : []
+    if (!offer.success) {
+      return []
+    }
+    const recordedByThisDrain = offersBeforeDrain
+      ? !offersBeforeDrain.has(offer.data.sessionId)
+      : offer.data.recordedAt >= drainStartedAt - CLOCK_SKEW_TOLERANCE_MS
+    return recordedByThisDrain ? [offer.data.sessionId] : []
   })
   const outcome = { offered: ids.length, continued: 0, skipped: 0, unsupported: false }
   for (let offset = 0; offset < ids.length; offset += MAX_RESTART_RESUME_SESSIONS) {
diff --git a/src/main/hosted-sandbox/hosted-session-lease-scheduler.ts b/src/main/hosted-sandbox/hosted-session-lease-scheduler.ts
index c1919a26ae3..f300a2b3c35 100644
--- a/src/main/hosted-sandbox/hosted-session-lease-scheduler.ts
+++ b/src/main/hosted-sandbox/hosted-session-lease-scheduler.ts
@@ -24,7 +24,12 @@ export type HostedSessionLeasePorts = {
   warn: (minutesLeft: HostedLeaseWarning) => void
   /** Re-pairs with the rebooted orcad; resolves once the runtime answers again. */
   reconnect: (ready: HostedEnvironmentReady) => Promise<void>
-  resumeAgents: (drainStartedAt: number) => Promise<HostedAgentAutoResumeOutcome>
+  resumeAgents: (
+    drainStartedAt: number,
+    offersBeforeDrain: ReadonlySet<string> | null
+  ) => Promise<HostedAgentAutoResumeOutcome>
+  /** The host's restart offers before the drain, so only the drain's own are continued. */
+  snapshotOffers?: () => Promise<ReadonlySet<string> | null>
   onSuspended: () => void
   /** Replaces the driver suspend, e.g. to run the window's ordinary Sleep for the workspace. */
   suspend?: () => Promise<void>
@@ -158,6 +163,7 @@ export class HostedSessionLeaseScheduler {
 
   private async rollover(reason: 'opportunistic' | 'forced'): Promise<void> {
     const { driver, handle } = this.ports
+    const offersBeforeDrain = (await this.ports.snapshotOffers?.().catch(() => null)) ?? null
     const drainStartedAt = this.now()
     this.log(`[orca-cloud] ${reason} rollover`)
     this.ports.onRolloverStateChange?.('restarting')
@@ -172,7 +178,7 @@ export class HostedSessionLeaseScheduler {
     }
     this.ports.onRolloverStateChange?.('running')
     try {
-      const outcome = await this.ports.resumeAgents(drainStartedAt)
+      const outcome = await this.ports.resumeAgents(drainStartedAt, offersBeforeDrain)
       this.log(
         `[orca-cloud] continued ${outcome.continued}/${outcome.offered} agents after rollover`
       )
diff --git a/src/main/hosted-sandbox/hosted-session-lease.test.ts b/src/main/hosted-sandbox/hosted-session-lease.test.ts
index 087dc8d1dcc..6c7a4c69b8d 100644
--- a/src/main/hosted-sandbox/hosted-session-lease.test.ts
+++ b/src/main/hosted-sandbox/hosted-session-lease.test.ts
@@ -1,6 +1,6 @@
 import { describe, expect, it, vi } from 'vitest'
 import type { HostedEnvironmentReady } from './hosted-environment-provider'
-import { autoResumeAgentsAfterRollover } from './hosted-agent-auto-resume'
+import { autoResumeAgentsAfterRollover, listRestartOfferIds } from './hosted-agent-auto-resume'
 import { createHostedSandboxControlPlaneClient } from './hosted-sandbox-control-plane-client'
 import { createHostedSandboxDriver, HOSTED_SANDBOX_CAPABILITIES } from './hosted-sandbox-driver'
 import { decideHostedLeaseAction, type HostedActivitySample } from './hosted-session-lease-policy'
@@ -102,7 +102,7 @@ describe('hosted session lease scheduler', () => {
     expect(await scheduler.tick()).toEqual({ kind: 'rollover', reason: 'forced' })
     expect(reconnect).toHaveBeenCalledTimes(1)
     expect(reconnect.mock.calls[0]?.[0].session.startedAt).toBe(now)
-    expect(resumeAgents).toHaveBeenCalledWith(created.session.deadlineAt)
+    expect(resumeAgents).toHaveBeenCalledWith(created.session.deadlineAt, null)
     // The new session is far from its cap, so the next tick does nothing drastic.
     expect((await scheduler.tick()).kind).not.toBe('rollover')
   })
@@ -150,14 +150,15 @@ describe('agent auto-resume after rollover', () => {
       if (method === 'agentSession.restartResumable') {
         return {
           sessions: [
-            { sessionId: 'old', recordedAt: 900 },
-            { sessionId: 'a', recordedAt: 1000 },
-            { sessionId: 'b', recordedAt: 1500 }
+            { sessionId: 'old', recordedAt: T0 - 10 * MIN },
+            // The host's clock runs 30 s behind this machine's: still this drain's offer.
+            { sessionId: 'a', recordedAt: T0 - 30_000 },
+            { sessionId: 'b', recordedAt: T0 + 500 }
           ]
         }
       }
       return { continued: [{ sessionId: 'a' }], skipped: ['b'] }
-    }, 1000)
+    }, T0)
     expect(calls).toEqual([
       { method: 'agentSession.restartResumable', params: undefined },
       { method: 'agentSession.restartContinue', params: { sessionIds: ['a', 'b'] } }
@@ -178,3 +179,33 @@ describe('agent auto-resume after rollover', () => {
     expect(call).toHaveBeenCalledTimes(1)
   })
 })
+
+describe('agent auto-resume with a pre-drain offer snapshot', () => {
+  it('continues only offers the host did not already hold, whatever the clocks say', async () => {
+    const offers = [
+      { sessionId: 'left-for-user', recordedAt: T0 + 5_000 },
+      { sessionId: 'this-drain', recordedAt: T0 - 9 * MIN }
+    ]
+    const calls: unknown[] = []
+    const call = async (method: string, params?: Record<string, unknown>) => {
+      calls.push({ method, params })
+      return method === 'agentSession.restartResumable' ? { sessions: offers } : { continued: [{}] }
+    }
+    const before = await listRestartOfferIds(async () => ({ sessions: [offers[0]] }))
+    expect(before).toEqual(new Set(['left-for-user']))
+    const outcome = await autoResumeAgentsAfterRollover(call, T0, before)
+    expect(calls).toContainEqual({
+      method: 'agentSession.restartContinue',
+      params: { sessionIds: ['this-drain'] }
+    })
+    expect(outcome.offered).toBe(1)
+  })
+
+  it('answers null when the host cannot list its offers', async () => {
+    await expect(
+      listRestartOfferIds(async () => {
+        throw new Error('down')
+      })
+    ).resolves.toBeNull()
+  })
+})
diff --git a/src/main/hosted-sandbox/hosted-session-registry.ts b/src/main/hosted-sandbox/hosted-session-registry.ts
index 59e7d4b8332..9150eb10afe 100644
--- a/src/main/hosted-sandbox/hosted-session-registry.ts
+++ b/src/main/hosted-sandbox/hosted-session-registry.ts
@@ -21,7 +21,7 @@ import { noteRecipeVmWakePairing } from '../ephemeral-vm/recipe-vm-wake-pairings
 import { getEphemeralVmRecipeResultPairingCode } from '../../shared/ephemeral-vm-recipes'
 import { environmentHandleFromRecipeResult } from '../environment-providers/environment-provider-recipe-adapter'
 import type { HostedEnvironmentProviderDriver } from './hosted-environment-provider'
-import { autoResumeAgentsAfterRollover } from './hosted-agent-auto-resume'
+import { autoResumeAgentsAfterRollover, listRestartOfferIds } from './hosted-agent-auto-resume'
 import { HOSTED_SANDBOX_DRIVER_ID } from './hosted-sandbox-driver'
 import { createHostedRuntimeEnvironmentCall } from './hosted-runtime-environment-call'
 import type { HostedActivitySample } from './hosted-session-lease-policy'
@@ -137,7 +137,9 @@ export function createHostedSessionRegistry(deps: {
           true
         )
       },
-      resumeAgents: (drainStartedAt) => autoResumeAgentsAfterRollover(call, drainStartedAt),
+      snapshotOffers: () => listRestartOfferIds(call),
+      resumeAgents: (drainStartedAt, offersBeforeDrain) =>
+        autoResumeAgentsAfterRollover(call, drainStartedAt, offersBeforeDrain),
       onRolloverStateChange: (state) => {
         const event: HostedSessionStateEvent = { workspaceId: runtime.workspaceId ?? null, state }
         broadcast('orcaCloud:sessionState', event)
diff --git a/src/main/hosted-sandbox/hosted-workspace-runtime.ts b/src/main/hosted-sandbox/hosted-workspace-runtime.ts
index 931348febc4..b786880fc3e 100644
--- a/src/main/hosted-sandbox/hosted-workspace-runtime.ts
+++ b/src/main/hosted-sandbox/hosted-workspace-runtime.ts
@@ -5,6 +5,7 @@ import type { HostedSandboxControlPlaneClient } from './hosted-sandbox-control-p
 import type { EphemeralVmRuntimeRecord } from '../../shared/ephemeral-vm-runtimes'
 import type {
   CloudOomEvent,
+  CloudWakeProgressEvent,
   CloudWorkspaceErrorCode,
   CloudWorkspaceResult
 } from '../../shared/hosted-sandbox/cloud-workspace-api'
@@ -18,6 +19,7 @@ import {
 } from '../environment-providers/environment-provider-driver'
 import { environmentHandleFromRecipeResult } from '../environment-providers/environment-provider-recipe-adapter'
 import { isHostedEntitlementDenied } from './hosted-environment-provider'
+import { callRuntimeEnvironment } from '../ipc/runtime-environments/runtime-environment-transport-routing'
 import { HOSTED_SANDBOX_DRIVER_ID } from './hosted-sandbox-driver'
 import type { HostedWorkspaceService } from './hosted-workspace-service'
 
@@ -165,6 +167,83 @@ export function getHostedWorkspaceService(): HostedWorkspaceService | null {
   return current
 }
 
+/** Polls a cheap terminal listing until the woken server answers it (or the deadline passes). */
+export async function waitForTerminalsReachable(
+  userDataPath: string,
+  environmentId: string,
+  deadline: number,
+  stillWanted: () => boolean = () => true
+): Promise<boolean> {
+  while (Date.now() < deadline && stillWanted()) {
+    const remaining = deadline - Date.now()
+    // Bounded by the deadline: the probe neither waits past it on a wake in flight nor on a slow server.
+    const signal = AbortSignal.timeout(Math.max(1, remaining))
+    const response = await callRuntimeEnvironment(
+      userDataPath,
+      environmentId,
+      'terminal.list',
+      { limit: 1 },
+      Math.min(5_000, Math.max(1, remaining)),
+      undefined,
+      undefined,
+      { signal, preparation: { recipeVmHoldMs: Math.max(0, remaining) } }
+    ).catch(() => null)
+    if (response?.ok) {
+      return stillWanted()
+    }
+    await new Promise((resolve) => setTimeout(resolve, 250))
+  }
+  return false
+}
+
+/**
+ * After a wake's step answers: `ready` once the runtime record says running AND the woken server
+ * answers a terminal listing (panes rebind to the restarted server's terminals a moment after
+ * running; keys typed before that are dropped by design). `failed` when it never answers. Nothing
+ * when this wake is no longer the current one (a newer wake, a failure or a Sleep took over).
+ */
+export async function announceWakeUsable(
+  userDataPath: string,
+  workspaceId: string,
+  startedAt: number,
+  hooks: { isCurrent: () => boolean; emit: (event: Omit<CloudWakeProgressEvent, 'at'>) => void },
+  timeoutMs = 60_000
+): Promise<void> {
+  const deadline = Date.now() + timeoutMs
+  const running = (): EphemeralVmRuntimeRecord | null => {
+    const runtime = findCloudRuntime(userDataPath, workspaceId)?.runtime
+    return runtime?.status === 'running' ? runtime : null
+  }
+  while (Date.now() < deadline && hooks.isCurrent()) {
+    const runtime = running()
+    if (runtime) {
+      const reachable = runtime.runtimeEnvironmentId
+        ? await waitForTerminalsReachable(
+            userDataPath,
+            runtime.runtimeEnvironmentId,
+            deadline,
+            hooks.isCurrent
+          )
+        : true
+      if (hooks.isCurrent() && running()) {
+        hooks.emit(
+          reachable
+            ? { workspaceId, phase: 'ready', source: 'open', startedAt }
+            : {
+                workspaceId,
+                phase: 'failed',
+                source: 'open',
+                startedAt,
+                message: 'The workspace did not answer after waking.'
+              }
+        )
+      }
+      return
+    }
+    await new Promise((resolve) => setTimeout(resolve, 250))
+  }
+}
+
 /** Whether the control plane says this workspace is archived; unknown counts as not archived. */
 export async function isArchivedOnControlPlane(
   userDataPath: string,
@@ -185,7 +264,9 @@ export async function isArchivedOnControlPlane(
 
 let archiveCheck: ((workspaceId: string) => Promise<boolean>) | null = null
 /** Installed with Orca Cloud; the wake path asks it before resuming a cloud workspace. */
-export function setCloudArchiveCheck(check: ((workspaceId: string) => Promise<boolean>) | null): void {
+export function setCloudArchiveCheck(
+  check: ((workspaceId: string) => Promise<boolean>) | null
+): void {
   archiveCheck = check
 }
 /** False when Orca Cloud is off in this build. */
diff --git a/src/main/hosted-sandbox/hosted-workspace-service.ts b/src/main/hosted-sandbox/hosted-workspace-service.ts
index 0acdc98fcb6..5a86ccb93e8 100644
--- a/src/main/hosted-sandbox/hosted-workspace-service.ts
+++ b/src/main/hosted-sandbox/hosted-workspace-service.ts
@@ -18,7 +18,7 @@ import type {
 import { applyResumedRuntimePairing } from '../ephemeral-vm/runtime-resume-pairing'
 import { noteRecipeVmWakePairing } from '../ephemeral-vm/recipe-vm-wake-pairings'
 import { invalidateRuntimeEnvironmentTransport } from '../ipc/runtime-environments/runtime-environments'
-import { autoResumeAgentsAfterRollover } from './hosted-agent-auto-resume'
+import { autoResumeAgentsAfterRollover, listRestartOfferIds } from './hosted-agent-auto-resume'
 import type { HostedSandboxControlPlaneClient } from './hosted-sandbox-control-plane-client'
 import { toReady } from './hosted-sandbox-driver'
 import { createHostedRuntimeEnvironmentCall } from './hosted-runtime-environment-call'
@@ -28,6 +28,7 @@ import {
   failure,
   findCloudRuntime,
   readCachedCheckouts,
+  announceWakeUsable,
   type CloudRuntime
 } from './hosted-workspace-runtime'
 
@@ -95,17 +96,11 @@ export function installHostedWorkspaceService(deps: {
   }
 
   /** The step answers before the window re-pairs; `ready` fires once the runtime record says running. */
-  async function announceReadyWhenRunning(workspaceId: string, startedAt: number): Promise<void> {
-    const deadline = Date.now() + 60_000
-    while (Date.now() < deadline && wakes.has(workspaceId)) {
-      const runtime = findCloudRuntime(deps.userDataPath, workspaceId)?.runtime
-      if (runtime?.status === 'running') {
-        service.emitWakeProgress({ workspaceId, phase: 'ready', source: 'open', startedAt })
-        return
-      }
-      await new Promise((resolve) => setTimeout(resolve, 250))
-    }
-  }
+  const announceReadyWhenRunning = (workspaceId: string, startedAt: number): Promise<void> =>
+    announceWakeUsable(deps.userDataPath, workspaceId, startedAt, {
+      isCurrent: () => wakes.get(workspaceId)?.startedAt === startedAt,
+      emit: (event) => service.emitWakeProgress(event)
+    })
 
   const service: HostedWorkspaceService = {
     emitWakeProgress(event) {
@@ -213,6 +208,11 @@ export function installHostedWorkspaceService(deps: {
       source: 'restart',
       startedAt
     })
+    const call = found.runtime.runtimeEnvironmentId
+      ? createHostedRuntimeEnvironmentCall(deps.userDataPath, found.runtime.runtimeEnvironmentId)
+      : null
+    // Offers the host already holds were left for the user; only this restart's are continued.
+    const offersBeforeDrain = call ? await listRestartOfferIds(call) : null
     // The scheduler holds the old session's deadline and would warn/roll over the new one; a fresh one starts on sync.
     deps.stopSession(found.sandboxId)
     try {
@@ -231,14 +231,10 @@ export function installHostedWorkspaceService(deps: {
         source: 'restart',
         startedAt
       })
-      if (found.runtime.runtimeEnvironmentId) {
+      if (call) {
         // Same continuation as a rollover: chats the restart interrupted carry on by themselves.
-        const call = createHostedRuntimeEnvironmentCall(
-          deps.userDataPath,
-          found.runtime.runtimeEnvironmentId
-        )
-        void autoResumeAgentsAfterRollover(call, startedAt).catch((error: unknown) =>
-          log(`[orca-cloud] auto-resume after restart failed: ${String(error)}`)
+        void autoResumeAgentsAfterRollover(call, startedAt, offersBeforeDrain).catch(
+          (error: unknown) => log(`[orca-cloud] auto-resume after restart failed: ${String(error)}`)
         )
       }
       return { ok: true, value: null }
diff --git a/src/main/hosted-sandbox/hosted-workspace-wake-ready.test.ts b/src/main/hosted-sandbox/hosted-workspace-wake-ready.test.ts
new file mode 100644
index 00000000000..73a810d260f
--- /dev/null
+++ b/src/main/hosted-sandbox/hosted-workspace-wake-ready.test.ts
@@ -0,0 +1,49 @@
+import { describe, expect, it, vi } from 'vitest'
+
+const runtimes: { status: string; runtimeEnvironmentId?: string }[] = []
+let listOk = true
+vi.mock('../ipc/runtime-environments/runtime-environment-transport-routing', () => ({
+  callRuntimeEnvironment: vi.fn(async () =>
+    listOk ? { ok: true, result: {} } : { ok: false, error: { code: 'x', message: 'x' } }
+  )
+}))
+vi.mock('../../shared/ephemeral-vm-runtime-store', () => ({
+  listEphemeralVmRuntimes: () =>
+    runtimes.map((r) => ({
+      ...r,
+      workspaceId: 'ws',
+      recipe: { provider: 'orca-cloud' },
+      recipeResult: {
+        schemaVersion: 1,
+        pairingCode: 'x',
+        projectRoot: '/p',
+        orcaCloud: { sandboxId: 'sbx_1' }
+      }
+    }))
+}))
+vi.mock('../environment-providers/environment-provider-recipe-adapter', () => ({
+  environmentHandleFromRecipeResult: () => ({ driverState: { sandboxId: 'sbx_1' } })
+}))
+
+describe('announceWakeUsable', () => {
+  it('emits ready once running and reachable', async () => {
+    const { announceWakeUsable } = await import('./hosted-workspace-runtime')
+    runtimes.splice(0, runtimes.length, { status: 'running', runtimeEnvironmentId: 'env' })
+    listOk = true
+    const emit = vi.fn()
+    await announceWakeUsable('/u', 'ws', 1, { isCurrent: () => true, emit }, 2_000)
+    expect(emit).toHaveBeenCalledWith(expect.objectContaining({ phase: 'ready', startedAt: 1 }))
+  })
+
+  it('emits failed when the server never answers, and nothing for a superseded wake', async () => {
+    const { announceWakeUsable } = await import('./hosted-workspace-runtime')
+    runtimes.splice(0, runtimes.length, { status: 'running', runtimeEnvironmentId: 'env' })
+    listOk = false
+    const emit = vi.fn()
+    await announceWakeUsable('/u', 'ws', 2, { isCurrent: () => true, emit }, 600)
+    expect(emit).toHaveBeenCalledWith(expect.objectContaining({ phase: 'failed' }))
+    const stale = vi.fn()
+    await announceWakeUsable('/u', 'ws', 3, { isCurrent: () => false, emit: stale }, 600)
+    expect(stale).not.toHaveBeenCalled()
+  })
+})
diff --git a/src/main/ipc/runtime-environments/runtime-environment-recipe-vm-wake.test.ts b/src/main/ipc/runtime-environments/runtime-environment-recipe-vm-wake.test.ts
index 6e3c5b7f1bb..13f7642f191 100644
--- a/src/main/ipc/runtime-environments/runtime-environment-recipe-vm-wake.test.ts
+++ b/src/main/ipc/runtime-environments/runtime-environment-recipe-vm-wake.test.ts
@@ -13,7 +13,7 @@ import type {
   RecipeVmOpening,
   RecipeVmState
 } from '../../runtime/workspaces/sleep/recipe-vm-operations'
-import { prepareRecipeVm } from './runtime-environment-recipe-vm-wake'
+import { holdForInFlightRecipeVmWake, prepareRecipeVm } from './runtime-environment-recipe-vm-wake'
 import { RemoteRuntimeClientError } from '../../../shared/remote-runtime/remote-runtime-client-error'
 import {
   forgetRecipeVmWakePairingsForTests,
@@ -131,6 +131,65 @@ describe('a request to a recipe VM environment', () => {
     }
   )
 
+  it('holds a request that does not open the workspace for an in-flight wake, outside its call slot', async () => {
+    recordVm('running')
+    ownerState = 'waking'
+    const awaitWake = vi.fn(async () => 'up' as const)
+    registerRecipeVmWaker({
+      state,
+      noteOpened: vi.fn(),
+      holdOpen,
+      awaitWake,
+      openEnvironment: async () => 'up'
+    })
+    await holdForInFlightRecipeVmWake(userDataPath, VM_ENVIRONMENT, 'terminal.list', 5_000)
+    expect(awaitWake).toHaveBeenCalledWith('workspace-of-vm-1', false, 5_000, undefined)
+    // Bounded by the caller's hold (0 = never wait) and never for an open (that wakes in its slot).
+    await holdForInFlightRecipeVmWake(userDataPath, VM_ENVIRONMENT, 'terminal.list', 5_000, {
+      preparation: { recipeVmHoldMs: 0 }
+    })
+    await holdForInFlightRecipeVmWake(userDataPath, VM_ENVIRONMENT, 'worktree.activate', 5_000)
+    expect(awaitWake).toHaveBeenCalledTimes(1)
+    expect(holdOpen).not.toHaveBeenCalled()
+    // Inside the slot the request is still answered at once from the owner's state.
+    await expect(codeOf('none')).resolves.toBe('runtime_environment_waking')
+  })
+
+  it('caps the hold at the in-flight maximum and does not wait on a VM that is not waking', async () => {
+    recordVm('running')
+    const awaitWake = vi.fn(async () => 'up' as const)
+    registerRecipeVmWaker({
+      state,
+      noteOpened: vi.fn(),
+      holdOpen,
+      awaitWake,
+      openEnvironment: async () => 'up'
+    })
+    await holdForInFlightRecipeVmWake(userDataPath, VM_ENVIRONMENT, 'terminal.list', 600_000)
+    expect(awaitWake).not.toHaveBeenCalled()
+    ownerState = 'waking'
+    await holdForInFlightRecipeVmWake(userDataPath, VM_ENVIRONMENT, 'terminal.list', 600_000)
+    expect(awaitWake).toHaveBeenCalledWith('workspace-of-vm-1', false, 60_000, undefined)
+  })
+
+  it('reports the pairing a wake it waited through left, for the caller fence', async () => {
+    recordVm('running')
+    ownerState = 'waking'
+    registerRecipeVmWaker({
+      state,
+      noteOpened: vi.fn(),
+      holdOpen,
+      awaitWake: async () => {
+        noteRecipeVmWakePairing(VM_ENVIRONMENT.id, 9, true)
+        return 'up' as const
+      },
+      openEnvironment: async () => 'up'
+    })
+    await expect(
+      holdForInFlightRecipeVmWake(userDataPath, VM_ENVIRONMENT, 'terminal.list', 5_000)
+    ).resolves.toEqual({ before: VM_ENVIRONMENT, wokenPairingRevision: 9 })
+  })
+
   // A phone gives up after 30 seconds, so its open is held for less.
 
   // A Disconnect made before the open holds: no client's open wakes the VM behind that server.
diff --git a/src/main/ipc/runtime-environments/runtime-environment-recipe-vm-wake.ts b/src/main/ipc/runtime-environments/runtime-environment-recipe-vm-wake.ts
index f906a8612f9..dda73c5db0c 100644
--- a/src/main/ipc/runtime-environments/runtime-environment-recipe-vm-wake.ts
+++ b/src/main/ipc/runtime-environments/runtime-environment-recipe-vm-wake.ts
@@ -14,6 +14,7 @@ import {
   RUNTIME_ENVIRONMENT_WAKE_FAILED_MESSAGE,
   RUNTIME_ENVIRONMENT_WAKING_ERROR_CODE,
   RUNTIME_ENVIRONMENT_WAKING_MESSAGE,
+  recipeVmWakeIntentFor,
   type RecipeVmWakeIntent
 } from '../../../shared/remote-runtime/recipe-vm-wake'
 import { getRecipeVmWaker } from '../../runtime/workspaces/sleep/recipe-vm-waker-registry'
@@ -117,6 +118,46 @@ export async function prepareRecipeVm(
   return UNCHANGED
 }
 
+/** How long a request that does not open the workspace waits for a wake already in flight. */
+export const RECIPE_VM_IN_FLIGHT_WAKE_HOLD_MS = 60_000
+
+/**
+ * Before a request that does not open the workspace takes its call slot: while the VM's wake is
+ * already underway (often just reconnecting), wait for it, up to `holdMs`, instead of being refused
+ * and never retried. Never starts a wake and never refuses: the request's own preparation decides
+ * what happens next (it is refused there if the wake failed or is still running).
+ */
+export async function awaitRecipeVmInFlightWake<E extends RecipeVmEnvironment>(
+  userDataPath: string,
+  environment: E,
+  holdMs: number,
+  signal?: AbortSignal
+): Promise<HeldRecipeVmWake<E> | null> {
+  const waker = getRecipeVmWaker()
+  if (holdMs <= 0 || !waker?.awaitWake) {
+    return null
+  }
+  const vm = recipeVmOf(userDataPath, environment)
+  if (!vm || waker.state(vm.workspaceId, vm.recordSuspended) !== 'waking') {
+    return null
+  }
+  const before = latestRecipeVmWake(environment.id)
+  await waker.awaitWake(vm.workspaceId, vm.recordSuspended, holdMs, signal).catch(() => undefined)
+  const woken = latestRecipeVmWake(environment.id)
+  // The wake this request waited through re-paired the server: the caller's fence names the pairing
+  // before it, exactly as for a request that woke the VM itself.
+  return woken !== before
+    ? { before: environment, wokenPairingRevision: woken?.pairingRevision ?? null }
+    : null
+}
+
+/** A wake a request waited through before taking its call slot: the record from before it and
+ *  the pairing it left. */
+export type HeldRecipeVmWake<E = RecipeVmEnvironment> = {
+  before: E
+  wokenPairingRevision: number | null
+}
+
 /** The pairing revision a recipe VM wake this request waited for left its server on, if any. */
 export type RecipeVmPreparation = { wokenPairingRevision: number | null }
 const UNCHANGED: RecipeVmPreparation = { wokenPairingRevision: null }
@@ -155,3 +196,27 @@ function refusal(outcome: Exclude<RecipeVmOpening, 'up'> | 'asleep'): RemoteRunt
       )
   }
 }
+
+/** A request that does not open the workspace waits (bounded by its own timeout and hold) for a wake
+ *  already in flight. Called before the request takes a per-environment call slot, so held
+ *  background requests never block an open. */
+export function holdForInFlightRecipeVmWake<E extends RecipeVmEnvironment>(
+  userDataPath: string,
+  environment: E,
+  method: string,
+  timeoutMs: number | undefined,
+  options?: { preparation?: { recipeVmHoldMs?: number }; signal?: AbortSignal }
+): Promise<HeldRecipeVmWake<E> | null> {
+  if (recipeVmWakeIntentFor(method) !== 'none') {
+    return Promise.resolve(null)
+  }
+  const holdMs = Math.min(
+    RECIPE_VM_IN_FLIGHT_WAKE_HOLD_MS,
+    options?.preparation?.recipeVmHoldMs ?? Infinity,
+    timeoutMs ?? DEFAULT_CALL_TIMEOUT_MS
+  )
+  return awaitRecipeVmInFlightWake(userDataPath, environment, holdMs, options?.signal)
+}
+
+/** The transport's default call timeout, which also bounds the hold for calls that set none. */
+const DEFAULT_CALL_TIMEOUT_MS = 15_000
diff --git a/src/main/ipc/runtime-environments/runtime-environment-request-preparation.test.ts b/src/main/ipc/runtime-environments/runtime-environment-request-preparation.test.ts
index 18e6360355c..38bc56ae4a8 100644
--- a/src/main/ipc/runtime-environments/runtime-environment-request-preparation.test.ts
+++ b/src/main/ipc/runtime-environments/runtime-environment-request-preparation.test.ts
@@ -56,3 +56,46 @@ describe('a request whose own recipe VM wake re-paired its server', () => {
     expect((await fence(1, 'before')).failure).toMatchObject({ ok: false })
   })
 })
+
+describe('a fenced request that waited through a wake already in flight', () => {
+  beforeEach(() => {
+    prepare.mockClear()
+    // By the time the request takes its slot the record already holds the new pairing; its own
+    // preparation woke nothing.
+    prepared.current = { environment: AFTER_WAKE, before: AFTER_WAKE, wokenPairingRevision: null }
+  })
+
+  const heldFence = (pairingRevision: number, wokenPairingRevision: number | null) =>
+    prepareFencedRuntimeRequest(
+      '/user-data',
+      'env-vm',
+      'terminal.list',
+      undefined,
+      { pairingRevision, runtimeId: 'before' },
+      undefined,
+      { before: BEFORE as never, wokenPairingRevision }
+    )
+
+  it('passes the pre-wake fence and then expects the pairing that wake made', async () => {
+    await expect(heldFence(1, 2)).resolves.toMatchObject({
+      failure: null,
+      expected: { pairingRevision: 2, runtimeId: undefined }
+    })
+  })
+
+  it('still refuses a caller fenced to an older pairing', async () => {
+    expect((await heldFence(0, 2)).failure).toMatchObject({ ok: false })
+    expect(prepare).not.toHaveBeenCalled()
+  })
+
+  it('without the held wake, the same call is refused as changed', async () => {
+    const result = await prepareFencedRuntimeRequest(
+      '/user-data',
+      'env-vm',
+      'terminal.list',
+      undefined,
+      { pairingRevision: 1, runtimeId: 'before' }
+    )
+    expect(result.failure).toMatchObject({ ok: false })
+  })
+})
diff --git a/src/main/ipc/runtime-environments/runtime-environment-request-preparation.ts b/src/main/ipc/runtime-environments/runtime-environment-request-preparation.ts
index 5c5cc54739a..e204f046db3 100644
--- a/src/main/ipc/runtime-environments/runtime-environment-request-preparation.ts
+++ b/src/main/ipc/runtime-environments/runtime-environment-request-preparation.ts
@@ -22,14 +22,17 @@ export async function prepareFencedRuntimeRequest(
   method: string,
   preparation: ManagedRuntimeCallPreparation | undefined,
   expected: Expected,
-  signal?: AbortSignal
+  signal?: AbortSignal,
+  /** A recipe VM wake this request waited through before its call slot: its fence is checked
+   *  against the record from before that wake, as for a wake the request made itself. */
+  heldWake?: { before: KnownRuntimeEnvironment; wokenPairingRevision: number | null }
 ): Promise<
   | { failure: Rpc.RuntimeRpcResponse<never> }
   | { failure: null; environment: KnownRuntimeEnvironment; expected: Expected }
 > {
   // A stale caller is refused before its request can wake (and re-pair) a VM.
   const stale = runtimeEnvironmentRevisionFailure(
-    resolveEnvironment(userDataPath, environmentId),
+    heldWake?.before ?? resolveEnvironment(userDataPath, environmentId),
     expected.pairingRevision,
     method,
     expected.runtimeId
@@ -44,7 +47,10 @@ export async function prepareFencedRuntimeRequest(
     method,
     signal
   )
-  const { environment, wokenPairingRevision: woken } = prepared
+  const { environment } = prepared
+  const woken = prepared.wokenPairingRevision ?? heldWake?.wokenPairingRevision ?? null
+  const before =
+    prepared.wokenPairingRevision !== null ? prepared.before : (heldWake?.before ?? prepared.before)
   const failure =
     woken === null
       ? runtimeEnvironmentRevisionFailure(
@@ -54,7 +60,7 @@ export async function prepareFencedRuntimeRequest(
           expected.runtimeId
         )
       : (runtimeEnvironmentRevisionFailure(
-          prepared.before,
+          before,
           expected.pairingRevision,
           method,
           expected.runtimeId
diff --git a/src/main/ipc/runtime-environments/runtime-environment-transport-routing.ts b/src/main/ipc/runtime-environments/runtime-environment-transport-routing.ts
index 0a4fcce7984..e0fec03129a 100644
--- a/src/main/ipc/runtime-environments/runtime-environment-transport-routing.ts
+++ b/src/main/ipc/runtime-environments/runtime-environment-transport-routing.ts
@@ -15,6 +15,7 @@ import {
   resolveManagedRuntimeEnvironment,
   type ManagedRuntimeCallPreparation
 } from './runtime-environment-managed-tunnel'
+import { markEnvironmentUsedFromResponse } from './runtime-environment-usage-marking'
 import { recordRuntimeEnvironmentUsage } from '../../../shared/remote-runtime/host-store/runtime-environment-usage-record'
 import type * as Rpc from '../../../shared/runtime-rpc-envelope'
 import '../../../shared/remote-runtime/requests/remote-runtime-request-socket'
@@ -23,6 +24,7 @@ import type { RemoteRuntimeTransportSubscription } from '../../../shared/remote-
 import { withRuntimeUnreachableHint } from './runtime-environment-unreachable-hint'
 import { decodeRuntimeEnvironmentSubscriptionEvents } from './runtime-environment-subscription-events'
 import { enqueueRuntimeCall } from './runtime-environment-call-queue'
+import { holdForInFlightRecipeVmWake } from './runtime-environment-recipe-vm-wake'
 import {
   sendRemoteRuntimeConnectionRequestAbortable,
   sendRemoteRuntimeRequestAbortable
@@ -80,6 +82,13 @@ export async function callRuntimeEnvironment(
     )
   }
   const environment = resolveEnvironment(userDataPath, selector)
+  const held = await holdForInFlightRecipeVmWake(
+    userDataPath,
+    environment,
+    method,
+    timeoutMs,
+    options
+  )
   // Connect failures reject; retain the dispatched endpoint for hints because queued re-pairing can change it.
   let endpoint = getPreferredPairedRuntimeConnection(environment).endpoint
   try {
@@ -96,7 +105,8 @@ export async function callRuntimeEnvironment(
             pairingRevision: expectedEnvironmentPairingRevision,
             runtimeId: options?.expectedEnvironmentRuntimeId
           },
-          options?.signal
+          options?.signal,
+          held ?? undefined
         )
         if (prepared.failure) {
           return prepared.failure
@@ -290,18 +300,6 @@ export async function subscribeRuntimeEnvironment(
   }
 }
 
-function markEnvironmentUsedFromResponse(
-  userDataPath: string,
-  environmentId: string,
-  response: Rpc.RuntimeRpcResponse<unknown>
-): void {
-  if (response.ok === true) {
-    recordRuntimeEnvironmentUsage(userDataPath, environmentId, {
-      runtimeId: response._meta.runtimeId
-    })
-  }
-}
-
 function shouldUseCachedRequestConnection(method: string): boolean {
   return method === 'terminal.send' || method === 'terminal.updateViewport'
 }
diff --git a/src/main/ipc/runtime-environments/runtime-environment-usage-marking.ts b/src/main/ipc/runtime-environments/runtime-environment-usage-marking.ts
new file mode 100644
index 00000000000..83472942edb
--- /dev/null
+++ b/src/main/ipc/runtime-environments/runtime-environment-usage-marking.ts
@@ -0,0 +1,15 @@
+import { recordRuntimeEnvironmentUsage } from '../../../shared/remote-runtime/host-store/runtime-environment-usage-record'
+import type * as Rpc from '../../../shared/runtime-rpc-envelope'
+
+/** A successful answer records which server process served the environment. */
+export function markEnvironmentUsedFromResponse(
+  userDataPath: string,
+  environmentId: string,
+  response: Rpc.RuntimeRpcResponse<unknown>
+): void {
+  if (response.ok === true) {
+    recordRuntimeEnvironmentUsage(userDataPath, environmentId, {
+      runtimeId: response._meta.runtimeId
+    })
+  }
+}
diff --git a/src/main/runtime/workspaces/sleep/recipe-vm-in-flight-wake.test.ts b/src/main/runtime/workspaces/sleep/recipe-vm-in-flight-wake.test.ts
new file mode 100644
index 00000000000..bcc6b8075ee
--- /dev/null
+++ b/src/main/runtime/workspaces/sleep/recipe-vm-in-flight-wake.test.ts
@@ -0,0 +1,30 @@
+import { describe, expect, it } from 'vitest'
+import { awaitInFlightWake, WorkspaceSleepRequests, type VmOperation } from './recipe-vm-operations'
+
+describe('awaitInFlightWake', () => {
+  it('answers at once for a VM that is up or asleep, without starting anything', async () => {
+    const sleeps = new WorkspaceSleepRequests()
+    await expect(awaitInFlightWake([], false, sleeps, 'w', 1000)).resolves.toBe('up')
+    await expect(awaitInFlightWake([], true, sleeps, 'w', 1000)).resolves.toBe('asleep')
+  })
+
+  it('waits for the wake already in flight', async () => {
+    let finish = (): void => {}
+    const settled = new Promise<void>((resolve) => {
+      finish = resolve
+    })
+    const pending: VmOperation[] = [{ kind: 'wake', settled }]
+    const answer = awaitInFlightWake(pending, false, new WorkspaceSleepRequests(), 'w', 5000)
+    finish()
+    await expect(answer).resolves.toBe('up')
+  })
+
+  it('ends slept when a Sleep is asked for while it waits, and waking when the hold runs out', async () => {
+    const sleeps = new WorkspaceSleepRequests()
+    const never: VmOperation[] = [{ kind: 'wake', settled: new Promise(() => {}) }]
+    const slept = awaitInFlightWake(never, false, sleeps, 'w', 5000)
+    sleeps.noteRequested('w')
+    await expect(slept).resolves.toBe('slept')
+    await expect(awaitInFlightWake(never, false, sleeps, 'w', 5)).resolves.toBe('waking')
+  })
+})
diff --git a/src/main/runtime/workspaces/sleep/recipe-vm-operations.ts b/src/main/runtime/workspaces/sleep/recipe-vm-operations.ts
index 00305978ffd..1778f20ef98 100644
--- a/src/main/runtime/workspaces/sleep/recipe-vm-operations.ts
+++ b/src/main/runtime/workspaces/sleep/recipe-vm-operations.ts
@@ -124,3 +124,26 @@ export async function holdOpenUntilUp(
     stopAbortWatch()
   }
 }
+
+/** Holds a request that does not open the workspace while the wake already in flight settles; a VM
+ *  that is not waking answers at once with where it stands. Never starts a wake. */
+export async function awaitInFlightWake(
+  pending: readonly VmOperation[],
+  recordSuspended: boolean,
+  sleepRequests: WorkspaceSleepRequests,
+  worktreeId: string,
+  timeoutMs: number,
+  signal?: AbortSignal
+): Promise<RecipeVmOpening | 'asleep'> {
+  signal?.throwIfAborted()
+  const state = vmStateOf(pending, recordSuspended)
+  if (state !== 'waking') {
+    return state === 'up' ? 'up' : 'asleep'
+  }
+  const sleep = sleepRequests.next(worktreeId)
+  try {
+    return await holdOpenUntilUp(pendingVmWake(pending), sleep.requested, timeoutMs, signal)
+  } finally {
+    sleep.stop()
+  }
+}
diff --git a/src/main/runtime/workspaces/sleep/recipe-vm-waker-registry.ts b/src/main/runtime/workspaces/sleep/recipe-vm-waker-registry.ts
index b2697ae0ecd..cead8b03c5e 100644
--- a/src/main/runtime/workspaces/sleep/recipe-vm-waker-registry.ts
+++ b/src/main/runtime/workspaces/sleep/recipe-vm-waker-registry.ts
@@ -15,6 +15,14 @@ export type RecipeVmWaker = {
     timeoutMs: number,
     signal?: AbortSignal
   ) => Promise<RecipeVmOpening>
+  /** Holds a request that does not open the workspace while a wake already in flight finishes;
+   *  never starts one. */
+  awaitWake?: (
+    workspaceId: string,
+    recordSuspended: boolean,
+    timeoutMs: number,
+    signal?: AbortSignal
+  ) => Promise<RecipeVmOpening | 'asleep'>
   /** Holds an open of the workspace behind a saved environment (id or name) for the CLI. */
   openEnvironment: (selector: string) => Promise<RecipeVmOpening>
 }
diff --git a/src/main/runtime/workspaces/sleep/runtime-workspace-sleep-operations.ts b/src/main/runtime/workspaces/sleep/runtime-workspace-sleep-operations.ts
index 69c4825efa5..d75bfe20c49 100644
--- a/src/main/runtime/workspaces/sleep/runtime-workspace-sleep-operations.ts
+++ b/src/main/runtime/workspaces/sleep/runtime-workspace-sleep-operations.ts
@@ -6,7 +6,7 @@ import type {
   WorkspaceSleepRequest
 } from '../../../../shared/workspace-sleep'
 import { WorkspaceSleepCoordinator } from './workspace-sleep-runtime'
-import type { RecipeVmOpening, RecipeVmState } from './recipe-vm-operations'
+import { awaitInFlightWake, type RecipeVmOpening, type RecipeVmState } from './recipe-vm-operations'
 import { dropStrandedSleepRecord } from '../../terminal/stop/worktree-sleep-resume-records'
 import type { RestoredPane } from '../../terminal/recovery/restored-pane-start'
 import type { SleepingAgentSessionRecord } from '../../../../shared/agent-session/lifecycle/agent-session-resume'
@@ -166,6 +166,18 @@ export abstract class RuntimeWorkspaceSleepOperations extends OrcaRuntimeWithRes
     return this.workspaceSleep.holdOpen(worktreeId, recordSuspended, timeoutMs, signal)
   }
 
+  /** Holds a request that does not open this workspace while its in-flight wake finishes. */
+  awaitWorkspaceVmWake(
+    worktreeId: string,
+    recordSuspended: boolean,
+    timeoutMs: number,
+    signal?: AbortSignal
+  ): Promise<RecipeVmOpening | 'asleep'> {
+    const pending = this.workspaceSleep.pendingVmOperations.get(worktreeId) ?? []
+    const sleeps = this.workspaceSleep.sleepRequests
+    return awaitInFlightWake(pending, recordSuspended, sleeps, worktreeId, timeoutMs, signal)
+  }
+
   /** The window opened a slept pane; main resumes it and the window attaches. */
   resumeSleptPane(pane: RestoredPane, automatic?: boolean): Promise<boolean> {
     return this.workspaceSleep.resumePane(pane, automatic)
diff --git a/src/main/runtime/workspaces/sleep/workspace-sleep-runtime.ts b/src/main/runtime/workspaces/sleep/workspace-sleep-runtime.ts
index 49b038d774b..dec406887b3 100644
--- a/src/main/runtime/workspaces/sleep/workspace-sleep-runtime.ts
+++ b/src/main/runtime/workspaces/sleep/workspace-sleep-runtime.ts
@@ -95,8 +95,9 @@ export class WorkspaceSleepCoordinator {
   private readonly reopenings = new Map<string, number>()
   private readonly vmOperations = new Map<string, Promise<void>>()
   /** The VM operations asked for per workspace, in order, until each settles. */
-  private readonly pendingVmOperations = new Map<string, VmOperation[]>()
-  private readonly sleepRequests = new WorkspaceSleepRequests()
+  /** Read by the in-flight wake hold (awaitInFlightWake); written only here. */
+  readonly pendingVmOperations = new Map<string, VmOperation[]>()
+  readonly sleepRequests = new WorkspaceSleepRequests()
 
   constructor(private readonly runtime: WorkspaceSleepRuntime) {}
 
diff --git a/src/main/startup/main-process-runtime-service.ts b/src/main/startup/main-process-runtime-service.ts
index 7b0405af786..38a5ae32e8a 100644
--- a/src/main/startup/main-process-runtime-service.ts
+++ b/src/main/startup/main-process-runtime-service.ts
@@ -128,13 +128,17 @@ export function initializeMainProcessRuntime(): OrcaRuntimeService {
         onRuntimeEnvironmentStatusPublished(trackRuntimeEnvironmentVerifiedTransitions(listener))
     },
     workspaceSleepPlatform: {
+      // Sleep's own calls and observations never wait on a wake in flight.
       callEnvironment: (environmentId, method, params, timeoutMs) =>
         callRuntimeEnvironment(
           getRuntimeEnvironmentRegistryRoot(),
           environmentId,
           method,
           params,
-          timeoutMs
+          timeoutMs,
+          undefined,
+          undefined,
+          { preparation: { recipeVmHoldMs: 0 } }
         ),
       ownsVm: (workspaceId) =>
         findWorkspaceEphemeralVmRuntime(app.getPath('userData'), workspaceId) !== undefined,
@@ -166,6 +170,8 @@ export function initializeMainProcessRuntime(): OrcaRuntimeService {
     noteOpened: (workspaceId) => runtime.noteWorkspaceReopened(workspaceId),
     holdOpen: (workspaceId, suspended, timeoutMs, signal) =>
       runtime.holdWorkspaceVmOpen(workspaceId, suspended, timeoutMs, signal),
+    awaitWake: (workspaceId, suspended, timeoutMs, signal) =>
+      runtime.awaitWorkspaceVmWake(workspaceId, suspended, timeoutMs, signal),
     openEnvironment: (selector) => {
       const root = getRuntimeEnvironmentRegistryRoot()
       return openRecipeVmEnvironment(root, resolveEnvironment(root, selector))
diff --git a/src/renderer/src/components/orca-cloud/CloudWakingOverlay.tsx b/src/renderer/src/components/orca-cloud/CloudWakingOverlay.tsx
index 924577d777f..2eee77ebe5f 100644
--- a/src/renderer/src/components/orca-cloud/CloudWakingOverlay.tsx
+++ b/src/renderer/src/components/orca-cloud/CloudWakingOverlay.tsx
@@ -127,7 +127,9 @@ export function CloudWakingOverlay({
           : wake.source === 'restart'
             ? t('orcaCloudWorkspace.announce.restarting', 'Restarting {{name}}.', { name })
             : wake.source === 'unarchive'
-              ? t('orcaCloudWorkspace.announce.unarchiving', 'Restoring {{name}} from archive.', { name })
+              ? t('orcaCloudWorkspace.announce.unarchiving', 'Restoring {{name}} from archive.', {
+                  name
+                })
               : t('orcaCloudWorkspace.announce.waking', 'Waking {{name}}.', { name })
       }
     >
diff --git a/src/renderer/src/components/orca-cloud/OrcaCloudWorkspace.fixture.tsx b/src/renderer/src/components/orca-cloud/OrcaCloudWorkspace.fixture.tsx
index 7cc31796e56..cbeef9ddcf8 100644
--- a/src/renderer/src/components/orca-cloud/OrcaCloudWorkspace.fixture.tsx
+++ b/src/renderer/src/components/orca-cloud/OrcaCloudWorkspace.fixture.tsx
@@ -44,7 +44,12 @@ const running: HostedWorkspaceStatus = {
   archive: null,
   checkedAt: NOW
 }
-const asleep: HostedWorkspaceStatus = { ...running, state: 'sleeping', metrics: null, uptimeMs: null }
+const asleep: HostedWorkspaceStatus = {
+  ...running,
+  state: 'sleeping',
+  metrics: null,
+  uptimeMs: null
+}
 const entry = (
   status: HostedWorkspaceStatus | null,
   over: Partial<CloudStatusEntry> = {}
@@ -100,7 +105,11 @@ export const panelUnresponsive = defineFixture({
 export const panelRestarting = defineFixture({
   width: 300,
   render: () => (
-    <Panel state="unresponsive" value={entry({ ...running, state: 'unresponsive' })} pending="restart" />
+    <Panel
+      state="unresponsive"
+      value={entry({ ...running, state: 'unresponsive' })}
+      pending="restart"
+    />
   )
 })
 
@@ -298,7 +307,7 @@ function IdleToast(): React.JSX.Element {
   return (
     <>
       <div className="h-[200px] bg-background" />
-      <Toaster position="top-left" toastOptions={{ className: "font-sans text-sm" }} />
+      <Toaster position="top-left" toastOptions={{ className: 'font-sans text-sm' }} />
     </>
   )
 }
diff --git a/src/renderer/src/components/orca-cloud/cloud-workspace-actions.ts b/src/renderer/src/components/orca-cloud/cloud-workspace-actions.ts
index 148823b6697..7a637867e5f 100644
--- a/src/renderer/src/components/orca-cloud/cloud-workspace-actions.ts
+++ b/src/renderer/src/components/orca-cloud/cloud-workspace-actions.ts
@@ -109,7 +109,9 @@ export function runArchiveCloudWorkspace(
     }, options.undoMs ?? ARCHIVE_UNDO_MS)
     toast(
       options.name
-        ? translate('orcaCloudWorkspace.archivingNamed', 'Archiving {{name}}…', { name: options.name })
+        ? translate('orcaCloudWorkspace.archivingNamed', 'Archiving {{name}}…', {
+            name: options.name
+          })
         : translate('orcaCloudWorkspace.archiving', 'Archiving workspace…'),
       {
         id: toastId,
diff --git a/src/renderer/src/components/orca-cloud/offline/CloudWorkspaceOfflineView.tsx b/src/renderer/src/components/orca-cloud/offline/CloudWorkspaceOfflineView.tsx
index bfcbe286e66..4c8c52fe50e 100644
--- a/src/renderer/src/components/orca-cloud/offline/CloudWorkspaceOfflineView.tsx
+++ b/src/renderer/src/components/orca-cloud/offline/CloudWorkspaceOfflineView.tsx
@@ -96,7 +96,9 @@ export function CloudWorkspaceOfflineView(props: CloudOfflineViewProps): React.J
             </TabsTrigger>
             <TabsTrigger value="changes">
               {t('components.orcaCloud.offline.tabChanges', 'Changes')}
-              {changeCount > 0 ? <span className="text-muted-foreground">{changeCount}</span> : null}
+              {changeCount > 0 ? (
+                <span className="text-muted-foreground">{changeCount}</span>
+              ) : null}
             </TabsTrigger>
           </TabsList>
           <TabsContent value="chat" className="flex min-h-0 flex-1 flex-col pt-3">
diff --git a/src/renderer/src/components/sidebar/workspace-actions/context-menu/WorktreeCloudTransferMenuItem.tsx b/src/renderer/src/components/sidebar/workspace-actions/context-menu/WorktreeCloudTransferMenuItem.tsx
index f5a387c913e..086eb415977 100644
--- a/src/renderer/src/components/sidebar/workspace-actions/context-menu/WorktreeCloudTransferMenuItem.tsx
+++ b/src/renderer/src/components/sidebar/workspace-actions/context-menu/WorktreeCloudTransferMenuItem.tsx
@@ -32,10 +32,7 @@ export function WorktreeCloudTransferMenuItem({
   return (
     <DropdownMenuItem onSelect={() => void runOrcaCloudTransferToLocal(worktreeId)}>
       <Laptop className="size-3.5" />
-      {t(
-        'auto.components.sidebar.WorktreeContextMenu.moveToThisComputer',
-        'Move to this computer'
-      )}
+      {t('auto.components.sidebar.WorktreeContextMenu.moveToThisComputer', 'Move to this computer')}
     </DropdownMenuItem>
   )
 }
diff --git a/src/renderer/src/components/terminal-pane/pty-connection/deferred-cold-restore-and-snapshot.ts b/src/renderer/src/components/terminal-pane/pty-connection/deferred-cold-restore-and-snapshot.ts
index 0c22d59bde5..d45980ceb60 100644
--- a/src/renderer/src/components/terminal-pane/pty-connection/deferred-cold-restore-and-snapshot.ts
+++ b/src/renderer/src/components/terminal-pane/pty-connection/deferred-cold-restore-and-snapshot.ts
@@ -1,3 +1,4 @@
+import { markInterruptedTurnContinued } from './startup/cold-restore-resume-startup'
 import { paneResumeRecord } from './startup/pane-resume-record'
 import { useAppStore } from '@/store/index'
 import type { PtyReplayDataMeta } from '../pty-transport/pty-transport-types'
@@ -34,6 +35,7 @@ export function bindDeferredColdRestoreAndSnapshot(session: ConnectPanePtySessio
     if (!startup || startup.resumeSource?.cancelled) {
       return false
     }
+    markInterruptedTurnContinued(startup.interruptedTurnKey)
     const state = useAppStore.getState()
     if (!session.pendingStartupCommand && session.shouldDeliverStartupViaTerminalPaste) {
       session.pendingStartupCommand = {
diff --git a/src/renderer/src/components/terminal-pane/pty-connection/reattach/deferred-session-reattach-connect.ts b/src/renderer/src/components/terminal-pane/pty-connection/reattach/deferred-session-reattach-connect.ts
index 46f8bb740ad..052a8b77862 100644
--- a/src/renderer/src/components/terminal-pane/pty-connection/reattach/deferred-session-reattach-connect.ts
+++ b/src/renderer/src/components/terminal-pane/pty-connection/reattach/deferred-session-reattach-connect.ts
@@ -1,5 +1,6 @@
 import {
   NOT_REOPENED,
+  markInterruptedTurnContinued,
   reopenPaneAfterMissingReattach
 } from '../startup/cold-restore-resume-startup'
 import { writeStartupCwdFallbackNotice } from '../startup/startup-cwd-fallback-notice'
@@ -134,6 +135,10 @@ function connectDeferredSessionReattach(
   )
   session.beginReattachLiveDataDeferral(outputCallbacks.generation)
   session.transportConnectInFlightSince = Date.now()
+  // The command goes to the server now: a `continue` it carries is spent.
+  if (coldRestoreStartup?.command) {
+    markInterruptedTurnContinued(coldRestoreStartup.interruptedTurnKey)
+  }
   const reattachPromise = session.transport.connect({
     url: '',
     cols: session.cols,
diff --git a/src/renderer/src/components/terminal-pane/pty-connection/startup/cold-restore-continue.test.ts b/src/renderer/src/components/terminal-pane/pty-connection/startup/cold-restore-continue.test.ts
new file mode 100644
index 00000000000..16356718f15
--- /dev/null
+++ b/src/renderer/src/components/terminal-pane/pty-connection/startup/cold-restore-continue.test.ts
@@ -0,0 +1,62 @@
+import { describe, expect, it, vi } from 'vitest'
+
+vi.mock('@/store/index', () => ({ useAppStore: { getState: () => ({}) } }))
+
+describe('shouldContinueInterruptedTurn', () => {
+  const now = 1_800_000_000_000
+  const working = (stateStartedAt: number) => ({
+    state: 'working',
+    updatedAt: now - 1000,
+    stateStartedAt
+  })
+
+  it('continues a remote agent with a fresh working status, once per interrupted turn', async () => {
+    const { shouldContinueInterruptedTurn, interruptedTurnKey, markInterruptedTurnContinued } =
+      await import('./cold-restore-resume-startup')
+    const ctx = { paneKey: 'p1', hasSleepingRecord: false, now }
+    expect(shouldContinueInterruptedTurn(working(1), 'env-1', ctx)).toBe(true)
+    // Building (and discarding) the startup again does not spend the turn.
+    expect(shouldContinueInterruptedTurn(working(1), 'env-1', ctx)).toBe(true)
+    // Once the resume launched, a retried cold restore of the same turn does not send it again.
+    markInterruptedTurnContinued(interruptedTurnKey(working(1), 'p1'))
+    expect(shouldContinueInterruptedTurn(working(1), 'env-1', ctx)).toBe(false)
+    // A later interrupted turn does.
+    expect(shouldContinueInterruptedTurn(working(2), 'env-1', ctx)).toBe(true)
+  })
+
+  it('never continues after a deliberate sleep, for stale or non-working status, or locally', async () => {
+    const { shouldContinueInterruptedTurn } = await import('./cold-restore-resume-startup')
+    expect(
+      shouldContinueInterruptedTurn(working(10), 'env-1', {
+        paneKey: 'p2',
+        hasSleepingRecord: true,
+        now
+      })
+    ).toBe(false)
+    expect(
+      shouldContinueInterruptedTurn(
+        { state: 'working', updatedAt: now - 31 * 60_000, stateStartedAt: 11 },
+        'env-1',
+        {
+          paneKey: 'p3',
+          hasSleepingRecord: false,
+          now
+        }
+      )
+    ).toBe(false)
+    expect(
+      shouldContinueInterruptedTurn(
+        { state: 'waiting', updatedAt: now, stateStartedAt: 12 },
+        'env-1',
+        { paneKey: 'p4', hasSleepingRecord: false, now }
+      )
+    ).toBe(false)
+    expect(
+      shouldContinueInterruptedTurn(working(13), null, {
+        paneKey: 'p5',
+        hasSleepingRecord: false,
+        now
+      })
+    ).toBe(false)
+  })
+})
diff --git a/src/renderer/src/components/terminal-pane/pty-connection/startup/cold-restore-resume-startup.ts b/src/renderer/src/components/terminal-pane/pty-connection/startup/cold-restore-resume-startup.ts
index 983d4b9c96f..216ecb72b10 100644
--- a/src/renderer/src/components/terminal-pane/pty-connection/startup/cold-restore-resume-startup.ts
+++ b/src/renderer/src/components/terminal-pane/pty-connection/startup/cold-restore-resume-startup.ts
@@ -6,7 +6,10 @@ import { normalizeExecutionHostId } from '../../../../../../shared/execution-hos
 import { parseWorkspaceKey } from '../../../../../../shared/workspace-scope'
 import { useAppStore } from '@/store/index'
 import { createNonSecureContextUuid as createBrowserUuid } from '../../../../../../shared/non-secure-context-uuid'
-import { buildAgentResumeStartupPlan } from '../../../../../../shared/agent-launch/startup/tui-agent-resume-startup'
+import {
+  INTERRUPTED_TURN_CONTINUE_PROMPT,
+  buildAgentResumeStartupPlan
+} from '../../../../../../shared/agent-launch/startup/tui-agent-resume-startup'
 import {
   resolveRuntimeHostReportedPlatform,
   resolveRuntimeHostTerminalWindowsShell,
@@ -24,6 +27,7 @@ import {
   normalizeAgentProviderSession
 } from '../../../../../../shared/agent-session/lifecycle/agent-session-resume'
 
+import { AGENT_STATUS_STALE_AFTER_MS } from '../../../../../../shared/agent-status/contracts/agent-status-freshness'
 import type { HeldPaneReopenOutcome } from '../../session-restore/newer-daemon/newer-daemon-hold-state'
 import type { ColdRestoreAgentResumeStartup } from './fresh-spawn-types'
 
@@ -31,6 +35,45 @@ import type { ConnectPanePtySession } from '../connect-pane-pty-session'
 
 export const NOT_REOPENED: HeldPaneReopenOutcome = { reopened: false, agentResumed: false }
 
+/** Interrupted turns already continued, so a retried cold restore never sends `continue` twice. */
+const continuedInterruptedTurns = new Set<string>()
+
+/** Identity of the turn an agent was in when its host went away. */
+export function interruptedTurnKey(
+  entry: { updatedAt: number; stateStartedAt?: number },
+  paneKey: string
+): string {
+  return `${paneKey}\u0000${entry.stateStartedAt ?? entry.updatedAt}`
+}
+
+/** Called when a resume that carries `continue` actually launches (startups are often built and
+ *  discarded, e.g. on every reattach check). */
+export function markInterruptedTurnContinued(key: string | undefined): void {
+  if (key) {
+    continuedInterruptedTurns.add(key)
+  }
+}
+
+/**
+ * A cold-restored agent on a remote host whose last status was working lost its turn when the host
+ * restarted (reboot, crash, rollover): carry it on. Only with fresh evidence (a recent working
+ * status), never after a deliberate sleep (that leaves a sleeping record), once per interrupted turn.
+ * Local panes are left alone: their PTYs outlive app restarts.
+ */
+export function shouldContinueInterruptedTurn(
+  entry: { state: string; updatedAt: number; stateStartedAt?: number } | null | undefined,
+  runtimeEnvironmentId: string | null,
+  context: { paneKey: string; hasSleepingRecord: boolean; now?: number }
+): boolean {
+  if (!runtimeEnvironmentId || context.hasSleepingRecord || entry?.state !== 'working') {
+    return false
+  }
+  if ((context.now ?? Date.now()) - entry.updatedAt > AGENT_STATUS_STALE_AFTER_MS) {
+    return false
+  }
+  return !continuedInterruptedTurns.has(interruptedTurnKey(entry, context.paneKey))
+}
+
 type AppState = ReturnType<typeof useAppStore.getState>
 
 /** The agent session a cold restore of this pane would resume; read-only, so pre-spawn checks can share it. */
@@ -109,6 +152,12 @@ export function bindBuildColdRestoreAgentResumeStartup(session: ConnectPanePtySe
         session.executionHostId
       )
     })
+    const continueTurn =
+      entry !== null &&
+      shouldContinueInterruptedTurn(entry, session.transport.getRuntimeEnvironmentId?.() ?? null, {
+        paneKey: session.cacheKey,
+        hasSleepingRecord: Boolean(sleepingRecord)
+      })
     const startupPlan = buildAgentResumeStartupPlan({
       agent,
       providerSession,
@@ -117,7 +166,10 @@ export function bindBuildColdRestoreAgentResumeStartup(session: ConnectPanePtySe
       platform: resumeTarget.platform,
       agentHostPlatform: resumeTarget.agentHostPlatform,
       shell: resumeTarget.shell,
-      launchCwd: session.worktree?.path
+      launchCwd: session.worktree?.path,
+      // A remote host that restarted under a working agent (reboot, crash, VM rollover) killed it
+      // mid-turn; its last status still says working. Carry the turn on instead of waiting.
+      continuePrompt: continueTurn ? INTERRUPTED_TURN_CONTINUE_PROMPT : null
     })
     if (!startupPlan) {
       return null
@@ -151,6 +203,9 @@ export function bindBuildColdRestoreAgentResumeStartup(session: ConnectPanePtySe
           : {})
       },
       launchToken: coldRestoreLaunchToken,
+      ...(continueTurn && entry
+        ? { interruptedTurnKey: interruptedTurnKey(entry, session.cacheKey) }
+        : {}),
       useLiveEntry: Boolean(useLiveEntry),
       hasSleepingRecord: Boolean(sleepingRecord),
       sleepingRecordEntry
diff --git a/src/renderer/src/components/terminal-pane/pty-connection/startup/fresh-spawn-types.ts b/src/renderer/src/components/terminal-pane/pty-connection/startup/fresh-spawn-types.ts
index d3071dcc0a5..31926f92f3d 100644
--- a/src/renderer/src/components/terminal-pane/pty-connection/startup/fresh-spawn-types.ts
+++ b/src/renderer/src/components/terminal-pane/pty-connection/startup/fresh-spawn-types.ts
@@ -20,6 +20,8 @@ export type FreshSpawnOptions = {
 }
 
 export type ColdRestoreAgentResumeStartup = PendingStartupCommand & {
+  /** Set when the command carries `continue` for an interrupted turn; marked used on launch. */
+  interruptedTurnKey?: string
   agent: ResumableTuiAgent
   resumeProviderSession: AgentProviderSessionMetadata
   connectionId?: string | null
diff --git a/src/renderer/src/lib/orca-cloud/orca-cloud-workspace-state.test.ts b/src/renderer/src/lib/orca-cloud/orca-cloud-workspace-state.test.ts
index 4b26dcd5762..b19fa8f6c6b 100644
--- a/src/renderer/src/lib/orca-cloud/orca-cloud-workspace-state.test.ts
+++ b/src/renderer/src/lib/orca-cloud/orca-cloud-workspace-state.test.ts
@@ -14,7 +14,10 @@ import {
 } from './orca-cloud-workspace-state'
 
 const NOW = 1_800_000_000_000
-const status = (state: HostedWorkspaceStatus['state'], archive: HostedWorkspaceStatus['archive'] = null): HostedWorkspaceStatus => ({
+const status = (
+  state: HostedWorkspaceStatus['state'],
+  archive: HostedWorkspaceStatus['archive'] = null
+): HostedWorkspaceStatus => ({
   state,
   metrics: null,
   uptimeMs: null,
@@ -32,18 +35,39 @@ const wake = (phase: CloudWakeProgressEvent['phase'], at = NOW): CloudWakeProgre
 
 describe('deriveCloudDotState', () => {
   it('shows an in-flight wake over everything, including a sleeping desktop record', () => {
-    expect(deriveCloudDotState({ status: status('sleeping'), wake: wake('waking'), sleeping: true, now: NOW })).toBe('waking')
-    expect(deriveCloudDotState({ status: status('ready'), wake: wake('connecting'), sleeping: false, now: NOW })).toBe('waking')
+    expect(
+      deriveCloudDotState({
+        status: status('sleeping'),
+        wake: wake('waking'),
+        sleeping: true,
+        now: NOW
+      })
+    ).toBe('waking')
+    expect(
+      deriveCloudDotState({
+        status: status('ready'),
+        wake: wake('connecting'),
+        sleeping: false,
+        now: NOW
+      })
+    ).toBe('waking')
   })
 
   it('treats a wake with no terminal event for 4 minutes as stale', () => {
     expect(
-      deriveCloudDotState({ status: status('ready'), wake: wake('waking', NOW - 5 * 60_000), sleeping: false, now: NOW })
+      deriveCloudDotState({
+        status: status('ready'),
+        wake: wake('waking', NOW - 5 * 60_000),
+        sleeping: false,
+        now: NOW
+      })
     ).toBe('running')
   })
 
   it('archived beats the desktop sleep state; failed wakes show until stale', () => {
-    expect(deriveCloudDotState({ status: status('archived'), wake: undefined, sleeping: true, now: NOW })).toBe('archived')
+    expect(
+      deriveCloudDotState({ status: status('archived'), wake: undefined, sleeping: true, now: NOW })
+    ).toBe('archived')
     expect(
       deriveCloudDotState({
         status: status('sleeping', { archivedAt: NOW, expiresAt: null }),
@@ -52,16 +76,45 @@ describe('deriveCloudDotState', () => {
         now: NOW
       })
     ).toBe('archived')
-    expect(deriveCloudDotState({ status: status('sleeping'), wake: wake('failed'), sleeping: true, now: NOW })).toBe('failed')
+    expect(
+      deriveCloudDotState({
+        status: status('sleeping'),
+        wake: wake('failed'),
+        sleeping: true,
+        now: NOW
+      })
+    ).toBe('failed')
   })
 
   it('maps control-plane states; the local sleep record only fills in before the first read', () => {
-    expect(deriveCloudDotState({ status: status('ready'), wake: undefined, sleeping: false, now: NOW })).toBe('running')
-    expect(deriveCloudDotState({ status: status('unresponsive'), wake: undefined, sleeping: false, now: NOW })).toBe('unresponsive')
-    expect(deriveCloudDotState({ status: status('ready'), wake: undefined, sleeping: true, now: NOW })).toBe('running')
-    expect(deriveCloudDotState({ status: null, wake: undefined, sleeping: true, now: NOW })).toBe('sleeping')
-    expect(deriveCloudDotState({ status: status('provisioning'), wake: undefined, sleeping: false, now: NOW })).toBe('waking')
-    expect(deriveCloudDotState({ status: null, wake: undefined, sleeping: false, now: NOW })).toBe('unknown')
+    expect(
+      deriveCloudDotState({ status: status('ready'), wake: undefined, sleeping: false, now: NOW })
+    ).toBe('running')
+    expect(
+      deriveCloudDotState({
+        status: status('unresponsive'),
+        wake: undefined,
+        sleeping: false,
+        now: NOW
+      })
+    ).toBe('unresponsive')
+    expect(
+      deriveCloudDotState({ status: status('ready'), wake: undefined, sleeping: true, now: NOW })
+    ).toBe('running')
+    expect(deriveCloudDotState({ status: null, wake: undefined, sleeping: true, now: NOW })).toBe(
+      'sleeping'
+    )
+    expect(
+      deriveCloudDotState({
+        status: status('provisioning'),
+        wake: undefined,
+        sleeping: false,
+        now: NOW
+      })
+    ).toBe('waking')
+    expect(deriveCloudDotState({ status: null, wake: undefined, sleeping: false, now: NOW })).toBe(
+      'unknown'
+    )
   })
 })
 
diff --git a/src/renderer/src/lib/orca-cloud/orca-cloud-workspace-store-wake.test.ts b/src/renderer/src/lib/orca-cloud/orca-cloud-workspace-store-wake.test.ts
index 8dd132f0d6b..908f0ba2aae 100644
--- a/src/renderer/src/lib/orca-cloud/orca-cloud-workspace-store-wake.test.ts
+++ b/src/renderer/src/lib/orca-cloud/orca-cloud-workspace-store-wake.test.ts
@@ -19,7 +19,10 @@ const status = (state: HostedWorkspaceStatus['state']): HostedWorkspaceStatus =>
   checkedAt: 1
 })
 
-function stub(getStatus: OrcaCloudWorkspaceApi['getStatus'], ids: string[] = []): OrcaCloudWorkspaceApi {
+function stub(
+  getStatus: OrcaCloudWorkspaceApi['getStatus'],
+  ids: string[] = []
+): OrcaCloudWorkspaceApi {
   const bridge = {
     getStatus: vi.fn(getStatus),
     listCloudWorkspaceIds: vi.fn(async () => ids)
@@ -48,7 +51,13 @@ describe('wake state and archive guard', () => {
 
   it('a failed wake stays until dismissed', async () => {
     stub(async () => ({ ok: true, value: status('sleeping') }))
-    noteCloudWakeProgress({ workspaceId: 'a', phase: 'failed', source: 'open', startedAt: 1, at: 2 })
+    noteCloudWakeProgress({
+      workspaceId: 'a',
+      phase: 'failed',
+      source: 'open',
+      startedAt: 1,
+      at: 2
+    })
     expect(getCloudWorkspaceSnapshot().wake.a?.phase).toBe('failed')
     dismissCloudWake('a')
     expect(getCloudWorkspaceSnapshot().wake.a).toBeUndefined()
diff --git a/src/renderer/src/lib/orca-cloud/orca-cloud-workspace-store.test.ts b/src/renderer/src/lib/orca-cloud/orca-cloud-workspace-store.test.ts
index 06253c4a0e2..c679e2cb363 100644
--- a/src/renderer/src/lib/orca-cloud/orca-cloud-workspace-store.test.ts
+++ b/src/renderer/src/lib/orca-cloud/orca-cloud-workspace-store.test.ts
@@ -28,7 +28,7 @@ const ready: HostedWorkspaceStatus = {
   archive: null,
   checkedAt: 1
 }
-const ok = <T,>(value: T): CloudWorkspaceResult<T> => ({ ok: true, value })
+const ok = <T>(value: T): CloudWorkspaceResult<T> => ({ ok: true, value })
 
 function stubApi(overrides: Partial<OrcaCloudWorkspaceApi> = {}): OrcaCloudWorkspaceApi {
   const bridge: OrcaCloudWorkspaceApi = {
@@ -42,7 +42,9 @@ function stubApi(overrides: Partial<OrcaCloudWorkspaceApi> = {}): OrcaCloudWorks
     onOom: vi.fn(() => () => {}),
     ...overrides
   }
-  ;(globalThis as unknown as { window: { api: { orcaCloudWorkspace: OrcaCloudWorkspaceApi } } }).window = {
+  ;(
+    globalThis as unknown as { window: { api: { orcaCloudWorkspace: OrcaCloudWorkspaceApi } } }
+  ).window = {
     api: { orcaCloudWorkspace: bridge }
   }
   return bridge
@@ -66,7 +68,11 @@ describe('orca cloud workspace store', () => {
     const bridge = stubApi()
     await Promise.all([refreshCloudWorkspaceStatus('a'), refreshCloudWorkspaceStatus('a')])
     expect(bridge.getStatus).toHaveBeenCalledTimes(1)
-    bridge.getStatus = vi.fn(async () => ({ ok: false as const, code: 'unavailable' as const, message: 'down' }))
+    bridge.getStatus = vi.fn(async () => ({
+      ok: false as const,
+      code: 'unavailable' as const,
+      message: 'down'
+    }))
     await refreshCloudWorkspaceStatus('a')
     const entry = getCloudWorkspaceSnapshot().status.a!
     expect(entry.status?.state).toBe('ready')
@@ -75,7 +81,13 @@ describe('orca cloud workspace store', () => {
   })
 
   it('forgets a workspace the main process says is not cloud', async () => {
-    stubApi({ getStatus: vi.fn(async () => ({ ok: false as const, code: 'not_cloud' as const, message: 'no' })) })
+    stubApi({
+      getStatus: vi.fn(async () => ({
+        ok: false as const,
+        code: 'not_cloud' as const,
+        message: 'no'
+      }))
+    })
     seedCloudWorkspaceSnapshot({ ids: new Set(['a']) })
     await refreshCloudWorkspaceStatus('a')
     expect(getCloudWorkspaceSnapshot().ids.has('a')).toBe(false)
@@ -117,7 +129,13 @@ describe('orca cloud workspace store', () => {
 
   it('tracks wake progress (adding the id) and dismisses OOM notices up to the seen count', async () => {
     stubApi()
-    noteCloudWakeProgress({ workspaceId: 'c', phase: 'waking', source: 'message', startedAt: 1, at: 2 })
+    noteCloudWakeProgress({
+      workspaceId: 'c',
+      phase: 'waking',
+      source: 'message',
+      startedAt: 1,
+      at: 2
+    })
     expect(getCloudWorkspaceSnapshot().ids.has('c')).toBe(true)
     noteCloudOom({ workspaceId: 'c', oomKills: 1, victim: 'node', at: 3 })
     dismissCloudOom('c')
diff --git a/src/shared/agent-launch/startup/tui-agent-resume-continue.test.ts b/src/shared/agent-launch/startup/tui-agent-resume-continue.test.ts
new file mode 100644
index 00000000000..c8bb1747775
--- /dev/null
+++ b/src/shared/agent-launch/startup/tui-agent-resume-continue.test.ts
@@ -0,0 +1,43 @@
+import { describe, expect, it } from 'vitest'
+import { buildAgentResumeStartupPlan } from './tui-agent-resume-startup'
+
+const providerSession = { key: 'session_id', id: 'claude-session-1' } as const
+
+describe('resume with a continue prompt', () => {
+  const base = { cmdOverrides: {}, platform: 'linux' as const, shell: 'posix' as const }
+
+  it('submits the prompt on resume for Claude and Codex', () => {
+    const claude = buildAgentResumeStartupPlan({
+      ...base,
+      agent: 'claude',
+      providerSession,
+      continuePrompt: 'continue'
+    })
+    expect(claude?.launchCommand).toMatch(/'?--resume'? '?claude-session-1'? '?continue'?$/)
+    const codex = buildAgentResumeStartupPlan({
+      ...base,
+      agent: 'codex',
+      providerSession: { key: 'session_id', id: 'codex-1' },
+      continuePrompt: 'continue'
+    })
+    expect(codex?.launchCommand).toMatch(/'?resume'? '?codex-1'? '?continue'?$/)
+  })
+
+  it('leaves other agents and empty prompts unchanged', () => {
+    const plain = buildAgentResumeStartupPlan({ ...base, agent: 'claude', providerSession })
+    const blank = buildAgentResumeStartupPlan({
+      ...base,
+      agent: 'claude',
+      providerSession,
+      continuePrompt: '  '
+    })
+    expect(blank?.launchCommand).toBe(plain?.launchCommand)
+    const cursor = buildAgentResumeStartupPlan({
+      ...base,
+      agent: 'cursor',
+      providerSession: { key: 'conversation_id', id: 'c-1' },
+      continuePrompt: 'continue'
+    })
+    expect(cursor?.launchCommand).not.toMatch(/continue'?$/)
+  })
+})
diff --git a/src/shared/agent-launch/startup/tui-agent-resume-startup.ts b/src/shared/agent-launch/startup/tui-agent-resume-startup.ts
index 3f981d79664..a1f61d88365 100644
--- a/src/shared/agent-launch/startup/tui-agent-resume-startup.ts
+++ b/src/shared/agent-launch/startup/tui-agent-resume-startup.ts
@@ -37,6 +37,9 @@ export function buildAgentResumeStartupPlan(args: {
   fork?: boolean
   /** OS that runs the agent when `platform` only picks quoting; null when unreported. */
   agentHostPlatform?: NodeJS.Platform | null
+  /** First message the resumed session submits, e.g. to carry on a turn its host cut off. Only
+   *  agents whose resume takes a prompt argument (Claude, Codex) send it; others ignore it. */
+  continuePrompt?: string | null
 }): AgentStartupPlan | null {
   const resumeArgv = args.fork
     ? getAgentForkArgv(args.agent, args.providerSession)
@@ -45,10 +48,15 @@ export function buildAgentResumeStartupPlan(args: {
     return null
   }
   // Codex otherwise asks for its old folder, even if deleted (#17745). Keep before resume so argv removal preserves the folder choice.
-  const argv =
+  const withCwd =
     args.agent === 'codex' && args.resumeInLaunchCwd
       ? [resumeArgv[0], '-c', 'tui.resume_cwd=current', ...resumeArgv.slice(1)]
       : resumeArgv
+  const continuePrompt = args.continuePrompt?.trim()
+  const argv =
+    continuePrompt && !args.fork && RESUME_PROMPT_AGENTS.has(args.agent)
+      ? [...withCwd, continuePrompt]
+      : withCwd
   const shell = resolveStartupShell(args.platform, args.shell)
   // Why: Codex restores a resumed thread's saved permissions unless the launch passes one, so
   // replaying Orca's launch-time flag would undo a change made inside the session (#10886).
@@ -112,6 +120,12 @@ export function buildAgentResumeStartupPlan(args: {
   }
 }
 
+/** Agents whose resume command accepts a positional prompt it submits on start. */
+const RESUME_PROMPT_AGENTS: ReadonlySet<ResumableTuiAgent> = new Set(['claude', 'codex'])
+
+/** What a resumed agent is told when its host went away mid-turn (restart, reboot, crash). */
+export const INTERRUPTED_TURN_CONTINUE_PROMPT = 'continue'
+
 /** WSL panes start at a UNC path while the agent reports its Linux path. */
 function isSameFolder(agentCwd: string, launchCwd: string): boolean {
   const launchPath = parseWslUncPath(launchCwd)?.linuxPath ?? launchCwd