diff --git a/apps/desktop/e2e/mock-server.ts b/apps/desktop/e2e/mock-server.ts
index a198ff8989c..7b14b0ea8f4 100644
--- a/apps/desktop/e2e/mock-server.ts
+++ b/apps/desktop/e2e/mock-server.ts
@@ -23,8 +23,10 @@ export const MOCK_REPLY = 'Hello from the mock inference server! The full boot c
 export interface MockServerOptions {
   /** Pause the matching stream after its first token for session-switch E2E coverage. */
   holdFirstStreamForPrompt?: string
-/** Pause the first completion whose request JSON contains this text. */
+  /** Pause the first completion whose request JSON contains this text. */
 holdFirstCompletionContaining?: string
+/** Pause the first completion after another hold whose request JSON contains this text. */
+holdFirstCompletionContainingAfterHeldCompletion?: string
 /** Absolute sandbox path written by the verify-on-stop scripted tool call. */
 verificationWritePath?: string
 }
@@ -285,12 +287,20 @@ export function startMockServer(options: MockServerOptions = {}): Promise<MockSe
     let resolveHeldStreamStarted: (() => void) | null = null
     let releaseHeldStream: (() => void) | null = null
     let heldCompletionCount = 0
-    const heldStreamStarted = new Promise<void>(resolveHeld => {
-      resolveHeldStreamStarted = resolveHeld
-    })
-    const heldStreamReleased = new Promise<void>(resolveRelease => {
-      releaseHeldStream = resolveRelease
-    })
+    let heldCompletionAfterHeldCompletion = false
+    let heldStreamStarted: Promise<void>
+    let heldStreamReleased: Promise<void>
+
+    const resetHeldStreamGate = (): void => {
+      heldStreamStarted = new Promise<void>(resolveHeld => {
+        resolveHeldStreamStarted = resolveHeld
+      })
+      heldStreamReleased = new Promise<void>(resolveRelease => {
+        releaseHeldStream = resolveRelease
+      })
+    }
+
+    resetHeldStreamGate()
     const server = http.createServer((req, res) => {
       // CORS headers — the Electron renderer doesn't need them, but they
       // don't hurt and make the server usable from a browser context too.
@@ -355,6 +365,15 @@ export function startMockServer(options: MockServerOptions = {}): Promise<MockSe
             heldCompletionCount === 0 &&
             JSON.stringify(parsed).includes(options.holdFirstCompletionContaining),
           )
+          const holdThisCompletionAfterHeldCompletion = Boolean(
+            options.holdFirstCompletionContainingAfterHeldCompletion &&
+            heldCompletionCount === 1 &&
+            !heldCompletionAfterHeldCompletion &&
+            JSON.stringify(parsed).includes(options.holdFirstCompletionContainingAfterHeldCompletion),
+          )
+          if (holdThisCompletionAfterHeldCompletion) {
+            heldCompletionAfterHeldCompletion = true
+          }
 
           // Detect the interim-message test trigger: the user's message
           // contains a specific keyword. The mock walks through the
@@ -459,10 +478,11 @@ export function startMockServer(options: MockServerOptions = {}): Promise<MockSe
 
           if (stream) {
             const holdThisStream = Boolean(
-              options.holdFirstStreamForPrompt && typeof lastUserMessage?.content === 'string' &&
-                lastUserMessage.content.includes(options.holdFirstStreamForPrompt),
+              (typeof lastUserMessage?.content === 'string' && (
+                options.holdFirstStreamForPrompt && lastUserMessage.content.includes(options.holdFirstStreamForPrompt)
+              )),
             )
-            streamTextResponse(res, model, MOCK_REPLY, holdThisStream || holdThisCompletion ? () => {
+            streamTextResponse(res, model, MOCK_REPLY, holdThisStream || holdThisCompletion || holdThisCompletionAfterHeldCompletion ? () => {
               if (holdThisCompletion) {
                 heldCompletionCount++
               }
@@ -470,8 +490,10 @@ export function startMockServer(options: MockServerOptions = {}): Promise<MockSe
               return heldStreamReleased
             } : undefined)
           } else {
-            if (holdThisCompletion) {
-              heldCompletionCount++
+            if (holdThisCompletion || holdThisCompletionAfterHeldCompletion) {
+              if (holdThisCompletion) {
+                heldCompletionCount++
+              }
               resolveHeldStreamStarted?.()
               void heldStreamReleased.then(() => nonStreamingTextResponse(res, model, MOCK_REPLY))
             } else {
@@ -510,7 +532,10 @@ export function startMockServer(options: MockServerOptions = {}): Promise<MockSe
         receivedPrompts,
         waitForHeldStream: () => heldStreamStarted,
         waitForHeldCompletion: () => heldStreamStarted,
-        releaseHeldStream: () => releaseHeldStream?.(),
+        releaseHeldStream: () => {
+          releaseHeldStream?.()
+          resetHeldStreamGate()
+        },
         heldCompletionCount: () => heldCompletionCount,
         close: () =>
           new Promise((resolveClose, rejectClose) => {
diff --git a/apps/desktop/e2e/session-compression-and-queue-stop.spec.ts b/apps/desktop/e2e/session-compression-and-queue-stop.spec.ts
index f15b8d0befc..b427a52374e 100644
--- a/apps/desktop/e2e/session-compression-and-queue-stop.spec.ts
+++ b/apps/desktop/e2e/session-compression-and-queue-stop.spec.ts
@@ -144,3 +144,66 @@ auxiliary:
     expect(fixture.mock.heldCompletionCount()).toBe(1)
   })
 })
+
+test.describe('session compression handoff queueing', () => {
+  let fixture: MockBackendFixture
+
+  test.beforeEach(async () => {
+    fixture = await setupMockBackend({
+      modelContextLength: 64_000,
+      extraConfig: `compression:
+  threshold_tokens: 22000
+  protect_first_n: 0
+  protect_last_n: 1
+auxiliary:
+  compression:
+    provider: custom
+    model: mock-model`,
+      mockServer: {
+        holdFirstCompletionContaining: 'You are a summarization agent creating a context checkpoint.',
+        holdFirstCompletionContainingAfterHeldCompletion: 'E2E_POST_COMPACTION_RUNNING',
+      },
+    })
+    await waitForAppReady(fixture, 120_000)
+  })
+
+  test.afterEach(async () => {
+    await fixture?.cleanup()
+  })
+
+  test('queues an Enter-submitted prompt while the post-compression turn is still running', async ({}, testInfo) => {
+    const { mock, page } = fixture
+    const compressionTrigger = 'E2E_TRIGGER_AUTOMATIC_COMPACTION '.repeat(500)
+    const running = 'E2E_POST_COMPACTION_RUNNING'
+    const queued = 'E2E_QUEUED_AFTER_COMPACTION'
+    const primary = page.locator('[data-slot="composer-root"] button[type="submit"]')
+
+    // Cross the threshold, complete compaction, then start a separate normal
+    // turn. This mirrors the user-visible sequence rather than holding the
+    // turn that caused the compaction itself.
+    await pasteAndSend(page, 'E2E_POST_COMPACTION_HISTORY_ONE '.repeat(5))
+    await waitForTranscript(page, MOCK_REPLY)
+    await pasteAndSend(page, 'E2E_POST_COMPACTION_HISTORY_TWO '.repeat(5))
+    await waitForTranscript(page, MOCK_REPLY)
+    await pasteAndSend(page, compressionTrigger)
+    await mock.waitForHeldCompletion()
+    expect(mock.heldCompletionCount()).toBe(1)
+    await expect(page.getByRole('status', { name: 'Summarizing thread' }).last()).toBeVisible()
+
+    mock.releaseHeldStream()
+    await expect(page.getByText(MOCK_REPLY, { exact: true })).toHaveCount(4)
+
+    await pasteAndSend(page, running)
+    await mock.waitForHeldStream()
+
+    await expect(primary).toHaveAttribute('aria-label', 'Queue message')
+    await pasteAndSend(page, queued)
+
+    await expect(page.getByText('1 Queued')).toBeVisible()
+    expect(mock.receivedPrompts).not.toContain(queued)
+    await page.screenshot({ path: testInfo.outputPath('queued-after-compression-handoff.png') })
+
+    mock.releaseHeldStream()
+    await expect.poll(() => mock.receivedPrompts.filter(prompt => prompt === queued), { timeout: 30_000 }).toHaveLength(1)
+  })
+})