diff --git a/src/renderer/src/components/dashboard/AgentDashboardDrawer.focus.test.tsx b/src/renderer/src/components/dashboard/AgentDashboardDrawer.focus.test.tsx
new file mode 100644
index 00000000000..b7bdea79cd6
--- /dev/null
+++ b/src/renderer/src/components/dashboard/AgentDashboardDrawer.focus.test.tsx
@@ -0,0 +1,192 @@
+// @vitest-environment happy-dom
+
+import '@testing-library/jest-dom/vitest'
+import type { ComponentProps } from 'react'
+import { act, cleanup, render, screen, waitFor } from '@testing-library/react'
+import userEvent from '@testing-library/user-event'
+import { afterEach, beforeEach, describe, expect, it, vi } from 'vitest'
+import { useAppStore } from '@/store'
+import type { AgentKanbanBoard } from '../dashboard-popout/AgentKanbanBoard'
+
+const mocks = vi.hoisted(() => ({
+  activateAndRevealWorkspace: vi.fn(() => true),
+  activateTabAndFocusPane: vi.fn(),
+  openPopout: vi.fn().mockResolvedValue(undefined)
+}))
+
+vi.mock('@/lib/worktree-activation', () => ({
+  activateAndRevealWorkspace: mocks.activateAndRevealWorkspace
+}))
+vi.mock('@/lib/activate-tab-and-focus-pane', () => ({
+  activateTabAndFocusPane: mocks.activateTabAndFocusPane
+}))
+vi.mock('./useLiveDashboardSnapshot', () => ({
+  useLiveDashboardSnapshot: () => ({ generatedAt: 1, cards: [] })
+}))
+vi.mock('../dashboard-popout/AgentKanbanBoard', () => ({
+  AgentKanbanBoard: ({
+    onClose,
+    onRevealAgent,
+    headerActions
+  }: ComponentProps<typeof AgentKanbanBoard>) => (
+    <>
+      <input aria-label="Search agents" />
+      <button onClick={onClose}>Close dashboard</button>
+      <button
+        onClick={() =>
+          onRevealAgent?.({ repoId: 'repo', worktreeId: 'worktree', tabId: 'tab', leafId: 'leaf' })
+        }
+      >
+        Reveal agent
+      </button>
+      {headerActions}
+    </>
+  )
+}))
+vi.mock('./AgentDashboardSettingsMenu', () => ({
+  AgentDashboardSettingsMenu: ({ onSwitchToPopout }: { onSwitchToPopout: () => void }) => (
+    <button onClick={onSwitchToPopout}>Pop out</button>
+  )
+}))
+
+import { AgentDashboardDrawer } from './AgentDashboardDrawer'
+
+const initialState = useAppStore.getInitialState()
+
+beforeEach(() => {
+  vi.clearAllMocks()
+  mocks.activateAndRevealWorkspace.mockReturnValue(true)
+  useAppStore.setState({ agentDashboardDrawerOpen: false, sidebarOpen: true, sidebarWidth: 320 })
+  Object.defineProperty(window, 'api', {
+    configurable: true,
+    value: { dashboard: { openPopout: mocks.openPopout } }
+  })
+})
+
+afterEach(async () => {
+  cleanup()
+  // Radix schedules close autofocus after unmount, including cleanup.
+  await act(async () => {
+    await new Promise((resolve) => setTimeout(resolve, 0))
+  })
+  useAppStore.setState(initialState, true)
+  vi.restoreAllMocks()
+})
+
+function fixture(): ReturnType<typeof render> {
+  const open = (): void => useAppStore.getState().setAgentDashboardDrawerOpen(true)
+  return render(
+    <>
+      <button onClick={open}>Opener A</button>
+      <button onClick={open}>Opener B</button>
+      <input aria-label="Outside input" />
+      <AgentDashboardDrawer statusBarVisible />
+    </>
+  )
+}
+
+async function openFrom(name = 'Opener A'): Promise<HTMLElement> {
+  const opener = screen.getByRole('button', { name })
+  opener.focus()
+  await userEvent.keyboard('{Enter}')
+  expect(document.activeElement).toBe(opener)
+  screen.getByRole('textbox', { name: 'Search agents' }).focus()
+  return opener
+}
+
+async function closed(): Promise<void> {
+  await waitFor(() => expect(screen.queryByRole('textbox', { name: 'Search agents' })).toBeNull())
+  await act(async () => {
+    await new Promise((resolve) => setTimeout(resolve, 0))
+  })
+}
+
+describe('AgentDashboardDrawer focus return', () => {
+  it.each(['Escape', 'Close dashboard'])('returns to the opener after %s', async (dismiss) => {
+    fixture()
+    const opener = await openFrom()
+    await (dismiss === 'Escape'
+      ? userEvent.keyboard('{Escape}')
+      : userEvent.click(screen.getByRole('button', { name: dismiss })))
+    await closed()
+    expect(document.activeElement).toBe(opener)
+  })
+
+  it('keeps outside focus when the store closes the drawer', async () => {
+    fixture()
+    await openFrom()
+    const outside = screen.getByRole('textbox', { name: 'Outside input' })
+    outside.focus()
+    act(() => useAppStore.getState().setAgentDashboardDrawerOpen(false))
+    await closed()
+    expect(document.activeElement).toBe(outside)
+  })
+
+  it('lets the real outside pointerdown dismissal hand focus to its target', async () => {
+    fixture()
+    const opener = await openFrom()
+    const sheet = screen.getByRole('dialog', { name: 'Agents' })
+    vi.spyOn(sheet, 'getBoundingClientRect').mockReturnValue(new DOMRect(320, 40, 600, 600))
+    const outside = screen.getByRole('textbox', { name: 'Outside input' })
+    const returned: Event[] = []
+    opener.addEventListener('focus', (event) => returned.push(event))
+    await userEvent.pointer({
+      target: outside,
+      keys: '[MouseLeft]',
+      coords: { clientX: 1000, clientY: 100 }
+    })
+    await closed()
+    expect(document.activeElement).toBe(outside)
+    expect(returned).toHaveLength(0)
+    await userEvent.keyboard('focus-test')
+    expect(outside).toHaveValue('focus-test')
+  })
+
+  it('restores after store dismissal and captures the next opener', async () => {
+    fixture()
+    const first = await openFrom()
+    act(() => useAppStore.getState().setAgentDashboardDrawerOpen(false))
+    await closed()
+    expect(document.activeElement).toBe(first)
+    const second = await openFrom('Opener B')
+    await userEvent.keyboard('{Escape}')
+    await closed()
+    expect(document.activeElement).toBe(second)
+  })
+
+  it('does not let an old close callback take focus from a reopened drawer', async () => {
+    fixture()
+    await openFrom()
+    act(() => useAppStore.getState().setAgentDashboardDrawerOpen(false))
+    const second = screen.getByRole('button', { name: 'Opener B' })
+    second.focus()
+    act(() => useAppStore.getState().setAgentDashboardDrawerOpen(true))
+    const search = screen.getByRole('textbox', { name: 'Search agents' })
+    search.focus()
+    await act(async () => {
+      await new Promise((resolve) => setTimeout(resolve, 0))
+    })
+    expect(document.activeElement).toBe(search)
+    await userEvent.keyboard('{Escape}')
+    await closed()
+    expect(document.activeElement).toBe(second)
+  })
+
+  it.each([true, false])('restores only when agent reveal fails (success: %s)', async (success) => {
+    fixture()
+    const opener = await openFrom()
+    mocks.activateAndRevealWorkspace.mockReturnValue(success)
+    await userEvent.click(screen.getByRole('button', { name: 'Reveal agent' }))
+    await closed()
+    expect(document.activeElement === opener).toBe(!success)
+  })
+
+  it('leaves focus handoff to the popout', async () => {
+    fixture()
+    const opener = await openFrom()
+    await userEvent.click(screen.getByRole('button', { name: 'Pop out' }))
+    await closed()
+    expect(mocks.openPopout).toHaveBeenCalledOnce()
+    expect(document.activeElement).not.toBe(opener)
+  })
+})
diff --git a/src/renderer/src/components/dashboard/AgentDashboardDrawer.tsx b/src/renderer/src/components/dashboard/AgentDashboardDrawer.tsx
index 7e4a744d8b4..665295c835c 100644
--- a/src/renderer/src/components/dashboard/AgentDashboardDrawer.tsx
+++ b/src/renderer/src/components/dashboard/AgentDashboardDrawer.tsx
@@ -1,4 +1,4 @@
-import { useCallback, useEffect, useRef, useState } from 'react'
+import { useCallback, useEffect, useLayoutEffect, useRef, useState } from 'react'
 import { useAppStore } from '@/store'
 import type { AgentSubjectReadIntent } from '@/attention/agent-subject-read-actions'
 import { Sheet, SheetContent, SheetTitle } from '@/components/ui/sheet'
@@ -33,9 +33,11 @@ const AGENT_BOARD_ESCAPE_BLOCKING_OVERLAY_SELECTOR = [
 /** Mount only while open to keep live snapshot derivation off the closed path. */
 function AgentDashboardDrawerBody({
   onClose,
+  onFocusHandoff,
   onMenuOpenChange
 }: {
   onClose: () => void
+  onFocusHandoff: () => void
   onMenuOpenChange: (open: boolean) => void
 }): React.JSX.Element {
   const snapshot = useLiveDashboardSnapshot()
@@ -47,17 +49,20 @@ function AgentDashboardDrawerBody({
   }, [])
   const handleRevealAgent = useCallback(
     (args: AgentRevealArgs) => {
-      revealDashboardAgent(args)
-      onClose()
+      if (revealDashboardAgent(args)) {
+        onFocusHandoff()
+      } else {
+        onClose()
+      }
     },
-    [onClose]
+    [onClose, onFocusHandoff]
   )
 
   // Hand off to pop-out mode instead of retaining a drawer inconsistent with the setting.
   const handleSwitchToPopout = useCallback(() => {
-    onClose()
+    onFocusHandoff()
     void window.api.dashboard.openPopout?.()
-  }, [onClose])
+  }, [onFocusHandoff])
 
   return (
     <AgentKanbanBoard
@@ -92,11 +97,43 @@ export function AgentDashboardDrawer({
   const sidebarOpen = useAppStore((s) => s.sidebarOpen)
   const sidebarWidth = useAppStore((s) => s.sidebarWidth)
   const [menuOpen, setMenuOpen] = useState(false)
+  const boardRef = useRef<HTMLDivElement | null>(null)
+  const focusReturnRef = useRef<{ opener: HTMLElement | null; handoff: boolean }>({
+    opener: null,
+    handoff: false
+  })
+
+  // Capture per open transition: a reopen during the exit animation reuses the Sheet without open autofocus.
+  useLayoutEffect(() => {
+    if (!open) {
+      return
+    }
+    const focusReturn = focusReturnRef.current
+    focusReturn.handoff = false
+    const active = document.activeElement
+    if (!boardRef.current?.closest('[data-slot="sheet-content"]')?.contains(active)) {
+      focusReturn.opener = active instanceof HTMLElement && active !== document.body ? active : null
+    }
+  }, [open])
+
+  // No Radix trigger exists for this store-driven drawer, so return focus only when unmount dropped it to body.
+  const handleCloseAutoFocus = useCallback((event: Event) => {
+    event.preventDefault()
+    const { opener, handoff } = focusReturnRef.current
+    if (!handoff && (!document.activeElement || document.activeElement === document.body)) {
+      opener?.focus({ preventScroll: true })
+    }
+  }, [])
   // Radix does not report close for unmounted menus; reset or the next drawer open could block outside dismissal.
   const close = useCallback(() => {
     setMenuOpen(false)
     setOpen(false)
   }, [setOpen])
+  // Outside dismissal, agent reveal and pop-out move focus themselves.
+  const closeForFocusHandoff = useCallback(() => {
+    focusReturnRef.current.handoff = true
+    close()
+  }, [close])
   // Store-driven closes bypass close(); clear menu state for sidebar collapse and workspace-board exclusivity too.
   useEffect(() => {
     if (!open) {
@@ -112,13 +149,11 @@ export function AgentDashboardDrawer({
     },
     [setOpen]
   )
-  const boardRef = useRef<HTMLDivElement | null>(null)
-
   useWorkspaceKanbanOutsideDismiss({
     open,
     boardRef,
     preserveOpenForMenu: menuOpen,
-    onOpenChange: setOpen
+    onOpenChange: closeForFocusHandoff
   })
 
   useEffect(() => {
@@ -203,13 +238,18 @@ export function AgentDashboardDrawer({
           // Suppress default header focus, which reveals hover-style affordances without a pointer.
           event.preventDefault()
         }}
+        onCloseAutoFocus={handleCloseAutoFocus}
         onPointerDownOutside={guardSidebarInteraction}
         onInteractOutside={guardSidebarInteraction}
       >
         <SheetTitle className="sr-only">{translate('dashboardPopout.title', 'Agents')}</SheetTitle>
         {/* Closed SheetContent unmounts the live snapshot body, avoiding closed-path derivation. */}
         <div ref={boardRef} className="flex min-h-0 flex-1 flex-col">
-          <AgentDashboardDrawerBody onClose={close} onMenuOpenChange={setMenuOpen} />
+          <AgentDashboardDrawerBody
+            onClose={close}
+            onFocusHandoff={closeForFocusHandoff}
+            onMenuOpenChange={setMenuOpen}
+          />
         </div>
       </SheetContent>
     </Sheet>