diff --git a/src/vs/platform/agentHost/node/agentService.ts b/src/vs/platform/agentHost/node/agentService.ts
index bab9b35df50..11f8d6b7e91 100644
--- a/src/vs/platform/agentHost/node/agentService.ts
+++ b/src/vs/platform/agentHost/node/agentService.ts
@@ -1306,12 +1306,18 @@ export class AgentService extends Disposable implements IAgentService {
 	private async _awaitInitialProviderMigration(): Promise<void> {
 		const providers = [...this._providers.values()];
 		const results = await Promise.allSettled(providers.map(provider => this._initialProviderMigrations.get(provider.id) ?? Promise.resolve()));
+		const retries: Promise<void>[] = [];
 		for (let index = 0; index < results.length; index++) {
 			const result = results[index];
 			if (result.status === 'rejected') {
-				this._logService.warn(`[AgentService] initial provider catalogs: provider ${providers[index].id} failed and will be retried on the next signal`, result.reason);
+				const provider = providers[index];
+				this._logService.warn(`[AgentService] initial provider catalog for ${provider.id} was unavailable; retrying before listing sessions`, result.reason);
+				const retry = this._ensureLegacyChatsMigrated(provider, true);
+				this._initialProviderMigrations.set(provider.id, retry);
+				retries.push(retry);
 			}
 		}
+		await Promise.all(retries);
 	}
 
 	/**
@@ -1474,7 +1480,7 @@ export class AgentService extends Disposable implements IAgentService {
 		}
 		const sessions = await this._enumerateLegacyProviderSessions(provider);
 		if (sessions === undefined) {
-			return;
+			throw new Error(`Provider ${provider.id} cannot enumerate its native session catalog yet`);
 		}
 		const existing = new Map((await this._listRegisteredSessions()).map(session => [session.session.toString(), session.external]));
 		const migrationLimiter = new Limiter<IRegisteredSession | undefined>(4);
diff --git a/src/vs/platform/agentHost/test/node/agentService.test.ts b/src/vs/platform/agentHost/test/node/agentService.test.ts
index 996217099ca..c425b3ed923 100644
--- a/src/vs/platform/agentHost/test/node/agentService.test.ts
+++ b/src/vs/platform/agentHost/test/node/agentService.test.ts
@@ -3965,14 +3965,16 @@ suite('AgentService (node dispatcher)', () => {
 			assert.strictEqual(agent.listExternalChatsCalls, 1);
 		});
 
-		test('a discovery signal does not bypass completed legacy migration semantics', async () => {
+		test('listSessions rejects an unavailable migration catalog and retries it on the next call', async () => {
 			class NotYetMigratableAgent extends MockAgent {
 				migrationCalls = 0;
 				enumerable = false;
 			}
 			const svc = disposables.add(new AgentService(new NullLogService(), fileService, createSessionDataService(), { _serviceBrand: undefined } as IProductService, createNoopGitService()));
+			svc.configurationService.updateRootConfig({ [AgentHostShowExternalSessionsConfigKey]: AgentHostExternalSessionsMode.All });
 			const agent = disposables.add(new NotYetMigratableAgent('copilot'));
 			const legacy = AgentSession.uri('copilot', 'legacy-migration-not-ready');
+			(agent as unknown as { _sessions: Map<string, URI> })._sessions.set(AgentSession.id(legacy), legacy);
 			(agent as unknown as { listChatsToMigrate: () => Promise<readonly IAgentChatMetadata[] | undefined> }).listChatsToMigrate = async () => {
 				agent.migrationCalls++;
 				return agent.enumerable
@@ -3980,18 +3982,20 @@ suite('AgentService (node dispatcher)', () => {
 					: undefined;
 			};
 			svc.registerProvider(agent);
-			await svc.listSessions();
+			await assert.rejects(svc.listSessions(), /cannot enumerate its native session catalog yet/);
+			const callsAfterFailure = agent.migrationCalls;
 
 			agent.enumerable = true;
-			agent.fireDiscoveredChats([]);
 			await timeout(0);
-
+			const listed = await svc.listSessions();
 			assert.deepStrictEqual({
-				migrationCalls: agent.migrationCalls,
-				registered: (await svc.getRegisteredSessions()).map(session => session.toString()),
+				retriedBeforeFailure: callsAfterFailure > 1,
+				retriedAfterFailure: agent.migrationCalls > callsAfterFailure,
+				listed: listed.map(session => session.session.toString()),
 			}, {
-				migrationCalls: 1,
-				registered: [],
+				retriedBeforeFailure: true,
+				retriedAfterFailure: true,
+				listed: [legacy.toString()],
 			});
 		});