diff --git a/src/main/browser/browser-popup-adapter-compatibility.electron.test.ts b/src/main/browser/browser-popup-adapter-compatibility.electron.test.ts
index e13b927abfa..2dd05b30463 100644
--- a/src/main/browser/browser-popup-adapter-compatibility.electron.test.ts
+++ b/src/main/browser/browser-popup-adapter-compatibility.electron.test.ts
@@ -12,6 +12,7 @@ import {
   snapshots,
   status
 } from './browser-popup-compatibility-cdp-fixture'
+import { waitForHiddenFrameInput } from './hidden-frame-input-readiness-fixture'
 
 enablePopupAdapterProbe()
 setPopupFixtureEvidenceName('adapter-electron-evidence.json')
@@ -334,10 +335,9 @@ async function exerciseSandboxControls(
     const offset = status().adapterProbe?.length ?? 0
     await installSandboxFrame(page, sandbox, destination, kind)
     const initialReceipt = receipts.length
-    await page
-      .frameLocator('#sandbox-probe')
-      .locator('#open')
-      .click(kind === 'link' ? { modifiers: ['Shift'] } : {})
+    const open = page.frameLocator('#sandbox-probe').locator('#open')
+    await waitForHiddenFrameInput(open)
+    await open.click(kind === 'link' ? { modifiers: ['Shift'] } : {})
     if (path === 'adopted' && kind === 'link') {
       await expect
         .poll(() => eventsSince(offset).some((event) => event.event === 'createWindow-missing'))
diff --git a/src/main/browser/browser-popup-background-cdp-probe.ts b/src/main/browser/browser-popup-background-cdp-probe.ts
index 7fca368da63..27ad3a58b4f 100644
--- a/src/main/browser/browser-popup-background-cdp-probe.ts
+++ b/src/main/browser/browser-popup-background-cdp-probe.ts
@@ -2,6 +2,7 @@ import { mkdirSync } from 'node:fs'
 import { join } from 'node:path'
 import type { Page } from 'playwright'
 import { expect } from 'vitest'
+import { waitForHiddenFrameInput } from './hidden-frame-input-readiness-fixture'
 import {
   artifactDir,
   browser,
@@ -103,22 +104,8 @@ export async function clickBackgroundPopupProbe(
       ? page.frameLocator('#background-probe').locator('#background-open')
       : page.locator('#background-open')
   if (probe.context === 'opaque') {
-    // A hidden OOPIF can finish loading before browser input reaches its new frame.
-    await locator.evaluate((element) => {
-      element.removeAttribute('data-background-input-ready')
-      element.addEventListener('pointermove', (event) => {
-        if (event.isTrusted) {
-          element.setAttribute('data-background-input-ready', 'true')
-        }
-      })
-    })
     await page.locator('#background-gesture').click()
-    await expect
-      .poll(async () => {
-        await locator.hover()
-        return locator.getAttribute('data-background-input-ready')
-      })
-      .toBe('true')
+    await waitForHiddenFrameInput(locator)
     // Opaque frame input does not reach Electron's root route gesture gate.
     await page.locator('#background-gesture').click()
   }
diff --git a/src/main/browser/browser-popup-compatibility-cdp-fixture.ts b/src/main/browser/browser-popup-compatibility-cdp-fixture.ts
index 8b2ee9c0013..dbfa7c10826 100644
--- a/src/main/browser/browser-popup-compatibility-cdp-fixture.ts
+++ b/src/main/browser/browser-popup-compatibility-cdp-fixture.ts
@@ -12,7 +12,10 @@ import { build as buildVite } from 'vite'
 import { waitForBrowserCdpEndpoint } from './browser-session-ua-cdp-collector'
 import { popupFixtureHtml } from './browser-popup-compatibility-page-fixture'
 import { resolveElectronProbeLaunch } from './electron-probe-display-launch'
-import { startHiddenRendererFrameCapture } from './hidden-renderer-frame-capture-fixture'
+import {
+  HIDDEN_RENDERER_FIRST_FRAME_TIMEOUT_MS,
+  startHiddenRendererFrameCapture
+} from './hidden-renderer-frame-capture-fixture'
 
 // Hidden renderer startup and CDP events can exceed the default one-second poll on CI.
 vi.setConfig({ expect: { poll: { timeout: 10_000 } } })
@@ -214,7 +217,7 @@ beforeAll(async () => {
     stopFrameCaptures.set(
       page,
       await startHiddenRendererFrameCapture(page, (hasFrame) =>
-        waitForFixture(hasFrame, 45_000).catch((error: unknown) => {
+        waitForFixture(hasFrame, HIDDEN_RENDERER_FIRST_FRAME_TIMEOUT_MS).catch((error: unknown) => {
           throw new Error(`No first frame for ${name}`, { cause: error })
         })
       )
diff --git a/src/main/browser/browser-popup-native-compatibility.electron.test.ts b/src/main/browser/browser-popup-native-compatibility.electron.test.ts
index 94b00d601a8..cfe8fdb80a6 100644
--- a/src/main/browser/browser-popup-native-compatibility.electron.test.ts
+++ b/src/main/browser/browser-popup-native-compatibility.electron.test.ts
@@ -14,6 +14,7 @@ import {
   status,
   setPopupFixtureEvidenceName
 } from './browser-popup-compatibility-cdp-fixture'
+import { waitForHiddenFrameInput } from './hidden-frame-input-readiness-fixture'
 import { MIN_POPUP_CONTENT_HEIGHT, MIN_POPUP_CONTENT_WIDTH } from './popup-window-minimum-size'
 
 setPopupFixtureEvidenceName('native-electron-evidence.json')
@@ -312,14 +313,13 @@ describe('hidden Chromium native popup request compatibility', () => {
             },
             { targetOrigin, opaque, shift }
           )
+          const post = page.frameLocator('#frame-probe').locator('#frame-post')
           if (opaque) {
-            // Prime hidden Linux OOPIF hit testing and the route's root gesture gate.
+            await waitForHiddenFrameInput(post)
+            // Opaque frame input does not reach the route's root gesture gate.
             await page.locator('#frame-gesture').click()
           }
-          await page
-            .frameLocator('#frame-probe')
-            .locator('#frame-post')
-            .click(shift ? { modifiers: ['Shift'] } : {})
+          await post.click(shift ? { modifiers: ['Shift'] } : {})
           await expect
             .poll(() => receipts.slice(before).find((receipt) => receipt.path === '/frame-post'))
             .toMatchObject({
diff --git a/src/main/browser/hidden-frame-input-readiness-fixture.ts b/src/main/browser/hidden-frame-input-readiness-fixture.ts
new file mode 100644
index 00000000000..378c08a9472
--- /dev/null
+++ b/src/main/browser/hidden-frame-input-readiness-fixture.ts
@@ -0,0 +1,28 @@
+import type { Locator } from 'playwright'
+import { expect } from 'vitest'
+
+const READY_ATTRIBUTE = 'data-hidden-frame-input-ready'
+
+// A new sandboxed iframe runs in its own renderer and can finish loading before the browser routes
+// pointer input to it; until then Playwright's click lands on the parent and the frame sees nothing.
+export async function waitForHiddenFrameInput(target: Locator): Promise<void> {
+  await target.evaluate((element, attribute) => {
+    element.removeAttribute(attribute)
+    element.addEventListener('pointermove', (event) => {
+      if (event.isTrusted) {
+        element.setAttribute(attribute, 'true')
+      }
+    })
+  }, READY_ATTRIBUTE)
+  await expect
+    .poll(
+      async () => {
+        // Leave first so every hover is a fresh move the browser has to route again.
+        await target.page().mouse.move(0, 0)
+        await target.hover()
+        return target.getAttribute(READY_ATTRIBUTE)
+      },
+      { timeout: 10_000 }
+    )
+    .toBe('true')
+}
diff --git a/src/main/browser/hidden-renderer-frame-capture-fixture.ts b/src/main/browser/hidden-renderer-frame-capture-fixture.ts
index 8019bdd8e10..1df9095027e 100644
--- a/src/main/browser/hidden-renderer-frame-capture-fixture.ts
+++ b/src/main/browser/hidden-renderer-frame-capture-fixture.ts
@@ -1,5 +1,8 @@
 import type { Page } from 'playwright'
 
+// Setup-only budget: a cold runner's first frame took up to 14s across 28 measured runs.
+export const HIDDEN_RENDERER_FIRST_FRAME_TIMEOUT_MS = 45_000
+
 export async function startHiddenRendererFrameCapture(
   page: Page,
   waitForFirstFrame: (hasFrame: () => boolean) => Promise<void>
diff --git a/src/main/browser/popup-origin-chrome.electron.test.ts b/src/main/browser/popup-origin-chrome.electron.test.ts
index 566d0cb7173..4f0276da65e 100644
--- a/src/main/browser/popup-origin-chrome.electron.test.ts
+++ b/src/main/browser/popup-origin-chrome.electron.test.ts
@@ -8,7 +8,10 @@ import {
   createPopupIdentityProbeRoot,
   launchPopupIdentityProbe
 } from './popup-identity-electron-probe'
-import { startHiddenRendererFrameCapture } from './hidden-renderer-frame-capture-fixture'
+import {
+  HIDDEN_RENDERER_FIRST_FRAME_TIMEOUT_MS,
+  startHiddenRendererFrameCapture
+} from './hidden-renderer-frame-capture-fixture'
 
 type OriginProbeWindow = Window & { originProbeChild?: Window }
 
@@ -138,9 +141,11 @@ beforeAll(async () => {
   }
   page = found
   stopCapture = await startHiddenRendererFrameCapture(page, (hasFrame) =>
-    vi.waitFor(() => expect(hasFrame()).toBe(true), { timeout: 10_000 })
+    vi.waitFor(() => expect(hasFrame()).toBe(true), {
+      timeout: HIDDEN_RENDERER_FIRST_FRAME_TIMEOUT_MS
+    })
   )
-}, 60_000)
+}, 90_000)
 
 afterAll(async () => {
   for (const response of held) {