diff --git a/src/vs/workbench/contrib/chat/browser/pluginAutoUpdate.ts b/src/vs/workbench/contrib/chat/browser/pluginAutoUpdate.ts
index 712cb3c1d84954..a1c6e97a4244c4 100644
--- a/src/vs/workbench/contrib/chat/browser/pluginAutoUpdate.ts
+++ b/src/vs/workbench/contrib/chat/browser/pluginAutoUpdate.ts
@@ -64,6 +64,7 @@ export class PluginAutoUpdate extends Disposable implements IWorkbenchContributi
 	}
 
 	private async _triggerAutoUpdate(marketplaceIds: ReadonlySet<string>): Promise<void> {
+		await this._meteredConnectionService.whenInitialized;
 		if (this._store.isDisposed || this._updateInFlight || this._meteredConnectionService.isConnectionMetered) {
 			return;
 		}
diff --git a/src/vs/workbench/contrib/chat/common/plugins/pluginMarketplaceService.ts b/src/vs/workbench/contrib/chat/common/plugins/pluginMarketplaceService.ts
index ac3f0376b56078..cfd0b8d1515934 100644
--- a/src/vs/workbench/contrib/chat/common/plugins/pluginMarketplaceService.ts
+++ b/src/vs/workbench/contrib/chat/common/plugins/pluginMarketplaceService.ts
@@ -410,7 +410,7 @@ export class PluginMarketplaceService extends Disposable implements IPluginMarke
 
 		this._register(runWhenGlobalIdle(() => {
 			this._updateChecksInitialized = true;
-			this._scheduleUpdateCheck();
+			void this._initializeUpdateChecks();
 			this._register(Event.filter(
 				_configurationService.onDidChangeConfiguration,
 				e => e.affectsConfiguration(AutoUpdateConfigurationKey)
@@ -442,6 +442,13 @@ export class PluginMarketplaceService extends Disposable implements IPluginMarke
 		}));
 	}
 
+	private async _initializeUpdateChecks(): Promise<void> {
+		await this._meteredConnectionService.whenInitialized;
+		if (!this._store.isDisposed) {
+			this._scheduleUpdateCheck();
+		}
+	}
+
 	clearUpdatesAvailable(marketplaceIds?: ReadonlySet<string>): void {
 		const remaining = marketplaceIds
 			? new Set([...this._marketplacesWithUpdates.get()].filter(id => !marketplaceIds.has(id)))
@@ -878,6 +885,11 @@ export class PluginMarketplaceService extends Disposable implements IPluginMarke
 	}
 
 	private async _doRunUpdateCheck(): Promise<void> {
+		await this._meteredConnectionService.whenInitialized;
+		if (this._store.isDisposed) {
+			return;
+		}
+
 		if (this._meteredConnectionService.isConnectionMetered) {
 			return;
 		}
diff --git a/src/vs/workbench/contrib/chat/test/browser/plugins/pluginAutoUpdate.test.ts b/src/vs/workbench/contrib/chat/test/browser/plugins/pluginAutoUpdate.test.ts
index 663ae6ba2af01e..bda92afd3df700 100644
--- a/src/vs/workbench/contrib/chat/test/browser/plugins/pluginAutoUpdate.test.ts
+++ b/src/vs/workbench/contrib/chat/test/browser/plugins/pluginAutoUpdate.test.ts
@@ -4,6 +4,7 @@
  *--------------------------------------------------------------------------------------------*/
 
 import assert from 'assert';
+import { DeferredPromise } from '../../../../../../base/common/async.js';
 import { CancellationToken } from '../../../../../../base/common/cancellation.js';
 import { Emitter } from '../../../../../../base/common/event.js';
 import { Disposable } from '../../../../../../base/common/lifecycle.js';
@@ -45,9 +46,13 @@ suite('PluginAutoUpdate', () => {
 		clearUpdatesAvailableCalls: ReadonlySet<string>[];
 	}
 
-	function createContribution(stateOverrides?: Partial<MockState>, isConnectionMetered = false): { contribution: PluginAutoUpdate; state: MockState; meteredConnectionService: TestMeteredConnectionService } {
+	function createContribution(
+		stateOverrides?: Partial<MockState>,
+		isConnectionMetered = false,
+		whenInitialized: Promise<void> = Promise.resolve(),
+	): { contribution: PluginAutoUpdate; state: MockState; meteredConnectionService: TestMeteredConnectionService } {
 		const instantiationService = store.add(new TestInstantiationService());
-		const meteredConnectionService = store.add(new TestMeteredConnectionService(isConnectionMetered));
+		const meteredConnectionService = store.add(new TestMeteredConnectionService(isConnectionMetered, whenInitialized));
 
 		const state: MockState = {
 			marketplacesWithUpdates: observableValue<ReadonlySet<string>>('test.marketplacesWithUpdates', new Set()),
@@ -104,6 +109,21 @@ suite('PluginAutoUpdate', () => {
 		})), [{ silent: true, automatic: true, marketplaceIds: ['github:microsoft/plugins'] }]);
 	});
 
+	test('waits for connection state initialization before updating', async () => {
+		const initialized = new DeferredPromise<void>();
+		const { state } = createContribution(undefined, false, initialized.p);
+
+		state.marketplacesWithUpdates.set(new Set(['github:microsoft/plugins']), undefined);
+		await flushMicrotasks();
+		assert.strictEqual(state.updateAllCalls.length, 0);
+
+		initialized.complete();
+		await flushMicrotasks();
+		await flushMicrotasks();
+
+		assert.deepStrictEqual(state.updateAllCalls.map(call => [...call.marketplaceIds ?? []]), [['github:microsoft/plugins']]);
+	});
+
 	test('retains queued updates while metered and runs them when unmetered', async () => {
 		const { state, meteredConnectionService } = createContribution(undefined, true);
 
diff --git a/src/vs/workbench/contrib/chat/test/common/plugins/pluginMarketplaceService.test.ts b/src/vs/workbench/contrib/chat/test/common/plugins/pluginMarketplaceService.test.ts
index c3d08a30792784..432d075aa8614b 100644
--- a/src/vs/workbench/contrib/chat/test/common/plugins/pluginMarketplaceService.test.ts
+++ b/src/vs/workbench/contrib/chat/test/common/plugins/pluginMarketplaceService.test.ts
@@ -788,6 +788,41 @@ suite('PluginMarketplaceService - installed plugins lifecycle', () => {
 		assert.strictEqual(fetchCount, 1);
 	});
 
+	test('periodic update checking waits for metered connection initialization', async () => {
+		let runIdle: ((idle: IdleDeadline) => void) | undefined;
+		store.add(installFakeRunWhenIdle((_target, runner) => {
+			runIdle = runner;
+			return Disposable.None;
+		}));
+		const initialized = new DeferredPromise<void>();
+		const meteredConnectionService = store.add(new TestMeteredConnectionService(false, initialized.p));
+		let fetchCount = 0;
+		const service = createService({
+			meteredConnectionService,
+			pluginRepositoryService: {
+				fetchRepository: async () => {
+					fetchCount++;
+					return false;
+				},
+			},
+		});
+		service.addInstalledPlugin(
+			URI.file('/agent-plugins/github.com/microsoft/plugins/my-plugin'),
+			makePlugin('my-plugin', 'my-plugin'),
+		);
+
+		assert.ok(runIdle);
+		runIdle({ didTimeout: false, timeRemaining: () => 50 });
+		await timeout(0);
+		assert.strictEqual(fetchCount, 0);
+
+		initialized.complete();
+		await timeout(0);
+		await timeout(0);
+
+		assert.strictEqual(fetchCount, 1);
+	});
+
 	test('defers an overdue check until queued updates are acknowledged', async () => {
 		const updateCheckInterval = 24 * 60 * 60 * 1000;
 		const clock = sinon.useFakeTimers({ now: updateCheckInterval + 1 });
@@ -993,6 +1028,7 @@ suite('PluginMarketplaceService - installed plugins lifecycle', () => {
 		assert.ok(runIdle);
 		runIdle({ didTimeout: false, timeRemaining: () => 50 });
 		await timeout(0);
+		await timeout(0);
 		assert.deepStrictEqual(fetched, [deferredRef.canonicalId]);
 
 		await configurationService.setUserConfiguration(ChatConfiguration.StrictMarketplaces, [