diff --git a/.gitignore b/.gitignore
index 8d9e1a2ad5..b5799a6e94 100644
--- a/.gitignore
+++ b/.gitignore
@@ -69,3 +69,4 @@ worktrees/
 
 .env
 .cursor
+.codex/config.toml
diff --git a/src/renderer/components/MultiAgentTask.tsx b/src/renderer/components/MultiAgentTask.tsx
index a4d9372fb9..b65f4bd8cd 100644
--- a/src/renderer/components/MultiAgentTask.tsx
+++ b/src/renderer/components/MultiAgentTask.tsx
@@ -18,6 +18,7 @@ import { CornerDownLeft } from 'lucide-react';
 import { TooltipProvider, Tooltip, TooltipTrigger, TooltipContent } from './ui/tooltip';
 import { useAutoScrollOnTaskSwitch } from '@/hooks/useAutoScrollOnTaskSwitch';
 import { useTerminalViewportWheelForwarding } from '@/hooks/useTerminalViewportWheelForwarding';
+import { useTerminalSearch } from '@/hooks/useTerminalSearch';
 import { getTaskEnvVars } from '@shared/task/envVars';
 import { rpc } from '@/lib/rpc';
 import { useWorkspaceConnection } from '../hooks/useWorkspaceConnection';
@@ -28,6 +29,7 @@ import { formatCommentsForAgent } from '@/lib/formatCommentsForAgent';
 import { buildPromptInjectionPayload } from '@/lib/terminalInjection';
 import { TaskScopeProvider } from './TaskScopeContext';
 import TaskContextBadges from './TaskContextBadges';
+import { TerminalSearchOverlay } from './TerminalSearchOverlay';
 
 interface Props {
   task: Task;
@@ -473,8 +475,26 @@ const MultiAgentTask: React.FC<Props> = ({
 
   // Ref to control terminal focus and viewport scrolling imperatively.
   const activeTerminalRef = useRef<TerminalPaneHandle>(null);
+  const activeTerminalContainerRef = useRef<HTMLDivElement | null>(null);
   const handleTerminalViewportWheelForwarding =
     useTerminalViewportWheelForwarding(activeTerminalRef);
+  const activeTerminalId = variants[activeTabIndex]?.worktreeId
+    ? `${variants[activeTabIndex].worktreeId}-main`
+    : null;
+  const {
+    isSearchOpen,
+    searchQuery,
+    searchStatus,
+    searchInputRef,
+    closeSearch,
+    handleSearchQueryChange,
+    stepSearch,
+  } = useTerminalSearch({
+    terminalId: activeTerminalId,
+    containerRef: activeTerminalContainerRef,
+    enabled: Boolean(activeTerminalId),
+    onCloseFocus: () => activeTerminalRef.current?.focus(),
+  });
 
   // Auto-scroll and focus when task or active tab changes
   useEffect(() => {
@@ -637,7 +657,8 @@ const MultiAgentTask: React.FC<Props> = ({
                   onWheelCapture={handleTerminalViewportWheelForwarding}
                 >
                   <div
-                    className={`mx-auto h-full max-w-4xl overflow-hidden rounded-md ${
+                    ref={isActive ? activeTerminalContainerRef : undefined}
+                    className={`relative mx-auto h-full max-w-4xl overflow-hidden rounded-md ${
                       v.agent === 'mistral'
                         ? isDark
                           ? 'bg-[#202938]'
@@ -647,6 +668,16 @@ const MultiAgentTask: React.FC<Props> = ({
                           : 'bg-white'
                     }`}
                   >
+                    <TerminalSearchOverlay
+                      isOpen={isActive && isSearchOpen}
+                      fullWidth
+                      searchQuery={searchQuery}
+                      searchStatus={searchStatus}
+                      searchInputRef={searchInputRef}
+                      onQueryChange={handleSearchQueryChange}
+                      onStep={stepSearch}
+                      onClose={closeSearch}
+                    />
                     <TerminalPane
                       ref={isActive ? activeTerminalRef : undefined}
                       id={`${v.worktreeId}-main`}
diff --git a/src/test/renderer/useTerminalSearch.test.tsx b/src/test/renderer/useTerminalSearch.test.tsx
new file mode 100644
index 0000000000..f581c1c212
--- /dev/null
+++ b/src/test/renderer/useTerminalSearch.test.tsx
@@ -0,0 +1,114 @@
+import React, { useRef } from 'react';
+import { fireEvent, render, screen } from '@testing-library/react';
+import { describe, expect, it, vi, beforeEach } from 'vitest';
+import { useTerminalSearch } from '../../renderer/hooks/useTerminalSearch';
+
+const { mockGetSession } = vi.hoisted(() => ({
+  mockGetSession: vi.fn(),
+}));
+
+vi.mock('../../renderer/terminal/SessionRegistry', () => ({
+  terminalSessionRegistry: {
+    getSession: mockGetSession,
+  },
+}));
+
+function TestHarness({
+  enabled = true,
+  terminalId = 'terminal-1',
+}: {
+  enabled?: boolean;
+  terminalId?: string | null;
+}) {
+  const containerRef = useRef<HTMLDivElement | null>(null);
+  const {
+    isSearchOpen,
+    searchQuery,
+    searchStatus,
+    searchInputRef,
+    closeSearch,
+    handleSearchQueryChange,
+  } = useTerminalSearch({
+    terminalId,
+    containerRef,
+    enabled,
+  });
+
+  return (
+    <div>
+      <button type="button" data-testid="outside-focus">
+        Outside
+      </button>
+      <div ref={containerRef} data-testid="terminal-container">
+        <button type="button" data-testid="terminal-focus">
+          Terminal
+        </button>
+        {isSearchOpen ? (
+          <input
+            ref={searchInputRef}
+            data-testid="search-input"
+            value={searchQuery}
+            onChange={(event) => handleSearchQueryChange(event.target.value)}
+          />
+        ) : null}
+        <button type="button" data-testid="close-search" onClick={closeSearch}>
+          Close
+        </button>
+        <div data-testid="search-status">
+          {searchStatus.currentIndex}/{searchStatus.total}
+        </div>
+      </div>
+    </div>
+  );
+}
+
+describe('useTerminalSearch', () => {
+  beforeEach(() => {
+    mockGetSession.mockReset();
+  });
+
+  it('opens search when Ctrl+F is pressed while focus is inside the terminal container', () => {
+    mockGetSession.mockReturnValue({
+      search: vi.fn(() => ({ found: false, currentIndex: 0, total: 0 })),
+      clearSearch: vi.fn(),
+    });
+
+    render(<TestHarness />);
+
+    screen.getByTestId('terminal-focus').focus();
+    fireEvent.keyDown(window, { key: 'f', ctrlKey: true });
+
+    expect(screen.getByTestId('search-input')).toBeInTheDocument();
+  });
+
+  it('ignores Ctrl+F when focus is outside the terminal container', () => {
+    mockGetSession.mockReturnValue({
+      search: vi.fn(() => ({ found: false, currentIndex: 0, total: 0 })),
+      clearSearch: vi.fn(),
+    });
+
+    render(<TestHarness />);
+
+    screen.getByTestId('outside-focus').focus();
+    fireEvent.keyDown(window, { key: 'f', ctrlKey: true });
+
+    expect(screen.queryByTestId('search-input')).not.toBeInTheDocument();
+  });
+
+  it('runs a search against the active terminal session when the query changes', () => {
+    const search = vi.fn(() => ({ found: true, currentIndex: 1, total: 3 }));
+    mockGetSession.mockReturnValue({
+      search,
+      clearSearch: vi.fn(),
+    });
+
+    render(<TestHarness />);
+
+    screen.getByTestId('terminal-focus').focus();
+    fireEvent.keyDown(window, { key: 'f', ctrlKey: true });
+    fireEvent.change(screen.getByTestId('search-input'), { target: { value: 'error' } });
+
+    expect(search).toHaveBeenCalledWith('error', { direction: 'next', reset: true });
+    expect(screen.getByTestId('search-status')).toHaveTextContent('1/3');
+  });
+});