diff --git a/src/vs/sessions/contrib/chat/electron-browser/chat.contribution.ts b/src/vs/sessions/contrib/chat/electron-browser/chat.contribution.ts
index 4a4f1ab768ed9a..faf35588d1af6e 100644
--- a/src/vs/sessions/contrib/chat/electron-browser/chat.contribution.ts
+++ b/src/vs/sessions/contrib/chat/electron-browser/chat.contribution.ts
@@ -134,10 +134,10 @@ class SelectAgentsFolderContribution extends Disposable implements IWorkbenchCon
 	private async openExistingSession(sessionResource: URI): Promise<void> {
 		this.logService.info(`[AgentsHandoff] openExistingSession: target=${sessionResource.toString()}`);
 
-		// Wait for the workbench to be ready so the session list / providers
-		// have populated. Otherwise openSession can't find the session.
-		await this.lifecycleService.when(LifecyclePhase.Eventually);
-		this.logService.info('[AgentsHandoff] reached LifecyclePhase.Eventually');
+		// Wait until initial restore has started so opening the target can cancel it,
+		// without delaying the handoff until the intentionally deferred Eventually phase.
+		await this.lifecycleService.when(LifecyclePhase.Restored);
+		this.logService.info('[AgentsHandoff] reached LifecyclePhase.Restored');
 
 		// Fast path — already on the target session.
 		const current = this.sessionsService.activeSession.get();
diff --git a/src/vs/workbench/contrib/chat/browser/chat.shared.contribution.ts b/src/vs/workbench/contrib/chat/browser/chat.shared.contribution.ts
index a71ea05007d6e5..4dc3f87ba0067c 100644
--- a/src/vs/workbench/contrib/chat/browser/chat.shared.contribution.ts
+++ b/src/vs/workbench/contrib/chat/browser/chat.shared.contribution.ts
@@ -2389,6 +2389,13 @@ configurationRegistry.registerConfiguration({
 			description: nls.localize('chat.titleBar.openInAgentsWindow.enabled', "Controls whether the Open in Agents Window button is shown in the title bar."),
 			default: true,
 		},
+		[ChatConfiguration.OpenInAgentsWindowRevealCurrentSession]: {
+			type: 'boolean',
+			description: nls.localize('chat.experimental.openInAgentsWindow.revealCurrentSession', "Controls whether Open in Agents Window reveals the current local Agent Host session instead of opening a new session."),
+			default: false,
+			tags: ['experimental'],
+			experiment: { mode: 'auto' },
+		},
 		'chat.approvedAccountOrganizations': {
 			type: 'array',
 			items: { type: 'string' },
diff --git a/src/vs/workbench/contrib/chat/common/constants.ts b/src/vs/workbench/contrib/chat/common/constants.ts
index c89f0ee2f6f017..e7444a3c6ada3e 100644
--- a/src/vs/workbench/contrib/chat/common/constants.ts
+++ b/src/vs/workbench/contrib/chat/common/constants.ts
@@ -103,6 +103,7 @@ export enum ChatConfiguration {
 	GrowthNotificationEnabled = 'chat.growthNotification.enabled',
 	TitleBarSignInEnabled = 'chat.titleBar.signIn.enabled',
 	TitleBarOpenInAgentsWindowEnabled = 'chat.titleBar.openInAgentsWindow.enabled',
+	OpenInAgentsWindowRevealCurrentSession = 'chat.experimental.openInAgentsWindow.revealCurrentSession',
 
 	ChatCustomizationsStructuredPreviewEnabled = 'chat.customizations.structuredPreview.enabled',
 	ChatCustomizationsPromptMigrationEnabled = 'chat.customizations.promptMigration.enabled',
diff --git a/src/vs/workbench/contrib/chat/electron-browser/agentSessions/agentSessionsActions.ts b/src/vs/workbench/contrib/chat/electron-browser/agentSessions/agentSessionsActions.ts
index d3c7f201ffdaed..5a41c3fa412376 100644
--- a/src/vs/workbench/contrib/chat/electron-browser/agentSessions/agentSessionsActions.ts
+++ b/src/vs/workbench/contrib/chat/electron-browser/agentSessions/agentSessionsActions.ts
@@ -30,7 +30,7 @@ import { IWorkbenchContribution } from '../../../../common/contributions.js';
 import { CHAT_CATEGORY } from '../../browser/actions/chatActions.js';
 import { IChatWidgetService } from '../../browser/chat.js';
 import { ChatContextKeys } from '../../common/actions/chatContextKeys.js';
-import { SessionType } from '../../common/chatSessionsService.js';
+import { isLocalAgentHostTarget, SessionType } from '../../common/chatSessionsService.js';
 import { IChatViewTitleActionContext } from '../../common/actions/chatActions.js';
 import { getChatSessionType, isUntitledChatSession } from '../../common/model/chatUri.js';
 import { ChatInputNotificationActionKind, ChatInputNotificationSeverity, IChatInputNotificationService } from '../../browser/widget/input/chatInputNotificationService.js';
@@ -115,6 +115,20 @@ export class OpenWorkspaceInAgentsWindowTitleBarAction extends Action2 {
 	}
 
 	async run(accessor: ServicesAccessor): Promise<void> {
+		const configurationService = accessor.get(IConfigurationService);
+		const sessionResource = accessor.get(IChatWidgetService).lastFocusedWidget?.viewModel?.sessionResource;
+		if (configurationService.getValue<boolean>(ChatConfiguration.OpenInAgentsWindowRevealCurrentSession) === true
+			&& sessionResource
+			&& !isUntitledChatSession(sessionResource)
+			&& isLocalAgentHostTarget(getChatSessionType(sessionResource))) {
+			await accessor.get(ICommandService).executeCommand(
+				OpenChatSessionInAgentsWindowAction.ID,
+				{ agentsWindowOpenSource: AgentsWindowOpenSource.TitleBar },
+				sessionResource,
+			);
+			return;
+		}
+
 		await accessor.get(ICommandService).executeCommand(OPEN_WORKSPACE_IN_AGENTS_WINDOW_COMMAND_ID, { source: AgentsWindowOpenSource.TitleBar });
 	}
 }
diff --git a/src/vs/workbench/contrib/chat/test/electron-browser/agentSessionsActions.test.ts b/src/vs/workbench/contrib/chat/test/electron-browser/agentSessionsActions.test.ts
index ffaea1eb0df2ff..1ca5c950660bc0 100644
--- a/src/vs/workbench/contrib/chat/test/electron-browser/agentSessionsActions.test.ts
+++ b/src/vs/workbench/contrib/chat/test/electron-browser/agentSessionsActions.test.ts
@@ -8,13 +8,28 @@ import { encodeHex, VSBuffer } from '../../../../../base/common/buffer.js';
 import { DisposableStore } from '../../../../../base/common/lifecycle.js';
 import { Schemas } from '../../../../../base/common/network.js';
 import { URI } from '../../../../../base/common/uri.js';
-import { upcastPartial } from '../../../../../base/test/common/mock.js';
+import { mock, upcastPartial } from '../../../../../base/test/common/mock.js';
 import { ensureNoDisposablesAreLeakedInTestSuite } from '../../../../../base/test/common/utils.js';
+import { ICommandService } from '../../../../../platform/commands/common/commands.js';
+import { IConfigurationService } from '../../../../../platform/configuration/common/configuration.js';
+import { TestConfigurationService } from '../../../../../platform/configuration/test/common/testConfigurationService.js';
 import { TestInstantiationService } from '../../../../../platform/instantiation/test/common/instantiationServiceMock.js';
 import { INativeHostService, IOpenAgentsWindowOptions } from '../../../../../platform/native/common/native.js';
 import { AgentsWindowOpenSource } from '../../../../../platform/window/common/window.js';
 import { IWorkspaceContextService } from '../../../../../platform/workspace/common/workspace.js';
-import { OpenWorkspaceInAgentsWindowAction } from '../../electron-browser/agentSessions/agentSessionsActions.js';
+import { IChatWidget, IChatWidgetService } from '../../browser/chat.js';
+import { ChatConfiguration, OPEN_WORKSPACE_IN_AGENTS_WINDOW_COMMAND_ID } from '../../common/constants.js';
+import { IChatViewModel } from '../../common/model/chatViewModel.js';
+import { OpenChatSessionInAgentsWindowAction, OpenWorkspaceInAgentsWindowAction, OpenWorkspaceInAgentsWindowTitleBarAction } from '../../electron-browser/agentSessions/agentSessionsActions.js';
+
+class TestCommandService extends mock<ICommandService>() {
+	readonly calls: { readonly commandId: string; readonly args: readonly unknown[] }[] = [];
+
+	override async executeCommand<T = unknown>(commandId: string, ...args: unknown[]): Promise<T | undefined> {
+		this.calls.push({ commandId, args });
+		return undefined;
+	}
+}
 
 suite('OpenWorkspaceInAgentsWindowAction', () => {
 	const disposables = ensureNoDisposablesAreLeakedInTestSuite();
@@ -64,3 +79,64 @@ suite('OpenWorkspaceInAgentsWindowAction', () => {
 		}]);
 	});
 });
+
+suite('OpenWorkspaceInAgentsWindowTitleBarAction', () => {
+	const disposables = ensureNoDisposablesAreLeakedInTestSuite();
+
+	async function run(sessionResource: URI | undefined, revealCurrentSession = true) {
+		const instantiationService = disposables.add(new TestInstantiationService());
+		const commandService = new TestCommandService();
+		const configurationService = new TestConfigurationService({
+			[ChatConfiguration.OpenInAgentsWindowRevealCurrentSession]: revealCurrentSession,
+		});
+		instantiationService.stub(ICommandService, commandService);
+		instantiationService.stub(IConfigurationService, configurationService);
+		instantiationService.stub(IChatWidgetService, upcastPartial<IChatWidgetService>({
+			lastFocusedWidget: sessionResource ? upcastPartial<IChatWidget>({
+				viewModel: upcastPartial<IChatViewModel>({ sessionResource }),
+			}) : undefined,
+		}));
+
+		const action = new OpenWorkspaceInAgentsWindowTitleBarAction();
+		await instantiationService.invokeFunction(accessor => action.run(accessor));
+		return commandService.calls;
+	}
+
+	test('reveals a persisted local Agent Host session and otherwise opens a workspace draft', async () => {
+		const localSession = URI.from({ scheme: 'agent-host-claude', path: '/session' });
+
+		assert.deepStrictEqual({
+			localSession: await run(localSession),
+			disabled: await run(localSession, false),
+			untitledLocalSession: await run(URI.from({ scheme: 'agent-host-claude', path: '/untitled-session' })),
+			remoteSession: await run(URI.from({ scheme: 'remote-host-claude', path: '/session' })),
+			regularSession: await run(URI.from({ scheme: 'vscode-chat-session', path: '/session' })),
+			noSession: await run(undefined),
+		}, {
+			localSession: [{
+				commandId: OpenChatSessionInAgentsWindowAction.ID,
+				args: [{ agentsWindowOpenSource: AgentsWindowOpenSource.TitleBar }, localSession],
+			}],
+			disabled: [{
+				commandId: OPEN_WORKSPACE_IN_AGENTS_WINDOW_COMMAND_ID,
+				args: [{ source: AgentsWindowOpenSource.TitleBar }],
+			}],
+			untitledLocalSession: [{
+				commandId: OPEN_WORKSPACE_IN_AGENTS_WINDOW_COMMAND_ID,
+				args: [{ source: AgentsWindowOpenSource.TitleBar }],
+			}],
+			remoteSession: [{
+				commandId: OPEN_WORKSPACE_IN_AGENTS_WINDOW_COMMAND_ID,
+				args: [{ source: AgentsWindowOpenSource.TitleBar }],
+			}],
+			regularSession: [{
+				commandId: OPEN_WORKSPACE_IN_AGENTS_WINDOW_COMMAND_ID,
+				args: [{ source: AgentsWindowOpenSource.TitleBar }],
+			}],
+			noSession: [{
+				commandId: OPEN_WORKSPACE_IN_AGENTS_WINDOW_COMMAND_ID,
+				args: [{ source: AgentsWindowOpenSource.TitleBar }],
+			}],
+		});
+	});
+});