diff --git a/agentplatform/agent_engines/templates/adk.py b/agentplatform/agent_engines/templates/adk.py
index 0334091544..ff3aecbb90 100644
--- a/agentplatform/agent_engines/templates/adk.py
+++ b/agentplatform/agent_engines/templates/adk.py
@@ -1127,6 +1127,7 @@ def set_up(self):
             artifact_service=self._tmpl_attrs.get("artifact_service"),
             memory_service=self._tmpl_attrs.get("memory_service"),
             credential_service=self._tmpl_attrs.get("credential_service"),
+            auto_create_session=True,
         )
         self._tmpl_attrs["in_memory_session_service"] = InMemorySessionService()
         self._tmpl_attrs["in_memory_artifact_service"] = InMemoryArtifactService()
diff --git a/tests/unit/agentplatform/frameworks/test_frameworks_adk.py b/tests/unit/agentplatform/frameworks/test_frameworks_adk.py
index ad9caf5c42..d88cd56074 100644
--- a/tests/unit/agentplatform/frameworks/test_frameworks_adk.py
+++ b/tests/unit/agentplatform/frameworks/test_frameworks_adk.py
@@ -531,6 +531,67 @@ async def test_async_stream_query(
             events.append(event)
         assert len(events) == 1
 
+    def test_set_up_runner_auto_create_session_enabled(
+        self,
+        default_instrumentor_builder_mock: mock.Mock,
+        get_project_id_mock: mock.Mock,
+    ):
+        """The main runner opts into auto-creating missing sessions (b/537477760)."""
+        app = adk_template.AdkApp(agent=_TEST_AGENT)
+        app.set_up()
+        assert app._tmpl_attrs.get("runner").auto_create_session is True
+
+    @pytest.mark.asyncio
+    async def test_runner_auto_creates_missing_session(
+        self,
+        default_instrumentor_builder_mock: mock.Mock,
+        get_project_id_mock: mock.Mock,
+    ):
+        from google.adk.runners import Runner
+        from google.adk.sessions.in_memory_session_service import (
+            InMemorySessionService,
+        )
+
+        app = adk_template.AdkApp(agent=_TEST_AGENT)
+        app.set_up()
+        assert app._tmpl_attrs.get("runner").auto_create_session is True
+
+        app_name = app._tmpl_attrs.get("app_name")
+        session_service = InMemorySessionService()
+        runner = Runner(
+            agent=_TEST_AGENT,
+            app_name=app_name,
+            session_service=session_service,
+            auto_create_session=app._tmpl_attrs.get("runner").auto_create_session,
+        )
+        missing_session_id = "0000000000000000000"
+
+        # Sanity: the session does not exist yet.
+        assert (
+            await session_service.get_session(
+                app_name=app_name,
+                user_id=_TEST_USER_ID,
+                session_id=missing_session_id,
+            )
+            is None
+        )
+
+        session = await runner._get_or_create_session(
+            user_id=_TEST_USER_ID,
+            session_id=missing_session_id,
+        )
+
+        assert session is not None
+        assert session.id == missing_session_id
+        assert (
+            await session_service.get_session(
+                app_name=app_name,
+                user_id=_TEST_USER_ID,
+                session_id=missing_session_id,
+            )
+            is not None
+        )
+
     @pytest.mark.asyncio
     async def test_async_stream_query_with_empty_session_events(
         self,
diff --git a/tests/unit/vertex_adk/test_agent_engine_templates_adk.py b/tests/unit/vertex_adk/test_agent_engine_templates_adk.py
index b5d1185dfd..c80e96a5b5 100644
--- a/tests/unit/vertex_adk/test_agent_engine_templates_adk.py
+++ b/tests/unit/vertex_adk/test_agent_engine_templates_adk.py
@@ -429,6 +429,67 @@ async def test_async_stream_query(
             events.append(event)
         assert len(events) == 1
 
+    def test_set_up_runner_auto_create_session_enabled(
+        self,
+        default_instrumentor_builder_mock: mock.Mock,
+        get_project_id_mock: mock.Mock,
+    ):
+        """The main runner opts into auto-creating missing sessions (b/537477760)."""
+        app = agent_engines.AdkApp(agent=_TEST_AGENT)
+        app.set_up()
+        assert app._tmpl_attrs.get("runner").auto_create_session is True
+
+    @pytest.mark.asyncio
+    async def test_runner_auto_creates_missing_session(
+        self,
+        default_instrumentor_builder_mock: mock.Mock,
+        get_project_id_mock: mock.Mock,
+    ):
+        from google.adk.runners import Runner
+        from google.adk.sessions.in_memory_session_service import (
+            InMemorySessionService,
+        )
+
+        app = agent_engines.AdkApp(agent=_TEST_AGENT)
+        app.set_up()
+        assert app._tmpl_attrs.get("runner").auto_create_session is True
+
+        app_name = app._tmpl_attrs.get("app_name")
+        session_service = InMemorySessionService()
+        runner = Runner(
+            agent=_TEST_AGENT,
+            app_name=app_name,
+            session_service=session_service,
+            auto_create_session=app._tmpl_attrs.get("runner").auto_create_session,
+        )
+        missing_session_id = "0000000000000000000"
+
+        # Sanity: the session does not exist yet.
+        assert (
+            await session_service.get_session(
+                app_name=app_name,
+                user_id=_TEST_USER_ID,
+                session_id=missing_session_id,
+            )
+            is None
+        )
+
+        session = await runner._get_or_create_session(
+            user_id=_TEST_USER_ID,
+            session_id=missing_session_id,
+        )
+
+        assert session is not None
+        assert session.id == missing_session_id
+        assert (
+            await session_service.get_session(
+                app_name=app_name,
+                user_id=_TEST_USER_ID,
+                session_id=missing_session_id,
+            )
+            is not None
+        )
+
     @pytest.mark.asyncio
     @mock.patch.dict(
         os.environ,
diff --git a/tests/unit/vertex_adk/test_reasoning_engine_templates_adk.py b/tests/unit/vertex_adk/test_reasoning_engine_templates_adk.py
index 598ec89fd8..e956f06e1a 100644
--- a/tests/unit/vertex_adk/test_reasoning_engine_templates_adk.py
+++ b/tests/unit/vertex_adk/test_reasoning_engine_templates_adk.py
@@ -475,6 +475,63 @@ async def test_async_stream_query(self):
             events.append(event)
         assert len(events) == 1
 
+    def test_set_up_runner_auto_create_session_enabled(self):
+        """The main runner opts into auto-creating missing sessions (b/537477760)."""
+        app = reasoning_engines.AdkApp(
+            agent=Agent(name=_TEST_AGENT_NAME, model=_TEST_MODEL)
+        )
+        app.set_up()
+        assert app._tmpl_attrs.get("runner").auto_create_session is True
+
+    @pytest.mark.asyncio
+    async def test_runner_auto_creates_missing_session(self):
+        from google.adk.runners import Runner
+        from google.adk.sessions.in_memory_session_service import (
+            InMemorySessionService,
+        )
+
+        app = reasoning_engines.AdkApp(
+            agent=Agent(name=_TEST_AGENT_NAME, model=_TEST_MODEL)
+        )
+        app.set_up()
+        assert app._tmpl_attrs.get("runner").auto_create_session is True
+
+        app_name = app._tmpl_attrs.get("app_name")
+        session_service = InMemorySessionService()
+        runner = Runner(
+            agent=Agent(name=_TEST_AGENT_NAME, model=_TEST_MODEL),
+            app_name=app_name,
+            session_service=session_service,
+            auto_create_session=app._tmpl_attrs.get("runner").auto_create_session,
+        )
+        missing_session_id = "0000000000000000000"
+
+        # Sanity: the session does not exist yet.
+        assert (
+            await session_service.get_session(
+                app_name=app_name,
+                user_id=_TEST_USER_ID,
+                session_id=missing_session_id,
+            )
+            is None
+        )
+
+        session = await runner._get_or_create_session(
+            user_id=_TEST_USER_ID,
+            session_id=missing_session_id,
+        )
+
+        assert session is not None
+        assert session.id == missing_session_id
+        assert (
+            await session_service.get_session(
+                app_name=app_name,
+                user_id=_TEST_USER_ID,
+                session_id=missing_session_id,
+            )
+            is not None
+        )
+
     @pytest.mark.asyncio
     async def test_async_stream_query_with_empty_session_events(self):
         app = reasoning_engines.AdkApp(
diff --git a/vertexai/agent_engines/templates/adk.py b/vertexai/agent_engines/templates/adk.py
index 58cc8a719f..25af45c2dd 100644
--- a/vertexai/agent_engines/templates/adk.py
+++ b/vertexai/agent_engines/templates/adk.py
@@ -1092,6 +1092,7 @@ def set_up(self):
             session_service=self._tmpl_attrs.get("session_service"),
             artifact_service=self._tmpl_attrs.get("artifact_service"),
             memory_service=self._tmpl_attrs.get("memory_service"),
+            auto_create_session=True,
         )
         self._tmpl_attrs["in_memory_session_service"] = InMemorySessionService()
         self._tmpl_attrs["in_memory_artifact_service"] = InMemoryArtifactService()
diff --git a/vertexai/preview/reasoning_engines/templates/adk.py b/vertexai/preview/reasoning_engines/templates/adk.py
index ec9fea0d78..4138a69ecf 100644
--- a/vertexai/preview/reasoning_engines/templates/adk.py
+++ b/vertexai/preview/reasoning_engines/templates/adk.py
@@ -977,6 +977,7 @@ def set_up(self):
             artifact_service=self._tmpl_attrs.get("artifact_service"),
             memory_service=self._tmpl_attrs.get("memory_service"),
             app_name=self._tmpl_attrs.get("app_name"),
+            auto_create_session=True,
         )
         self._tmpl_attrs["in_memory_session_service"] = InMemorySessionService()
         self._tmpl_attrs["in_memory_artifact_service"] = InMemoryArtifactService()