diff --git a/devel-common/src/tests_common/pytest_plugin.py b/devel-common/src/tests_common/pytest_plugin.py
index 6401dedc29340..e2fd72495c10c 100644
--- a/devel-common/src/tests_common/pytest_plugin.py
+++ b/devel-common/src/tests_common/pytest_plugin.py
@@ -1950,7 +1950,7 @@ def set_dag(what: StartupDetails, dag_id: str, task: TaskSDKBaseOperator) -> Run
         )
         if hasattr(parse, "spy"):
             spy_agency.unspy(parse)
-        spy_agency.spy_on(parse, call_fake=lambda _: ti)
+        spy_agency.spy_on(parse, call_fake=lambda _, log: ti)
         return ti
 
     return set_dag
diff --git a/providers/openlineage/tests/unit/openlineage/extractors/test_manager.py b/providers/openlineage/tests/unit/openlineage/extractors/test_manager.py
index ab3cdd56008cd..d96e82dc1ad9b 100644
--- a/providers/openlineage/tests/unit/openlineage/extractors/test_manager.py
+++ b/providers/openlineage/tests/unit/openlineage/extractors/test_manager.py
@@ -423,7 +423,7 @@ def set_dag(what: StartupDetails, dag_id: str, task: BaseOperator) -> RuntimeTas
         )
         if hasattr(parse, "spy"):
             spy_agency.unspy(parse)
-        spy_agency.spy_on(parse, call_fake=lambda _: ti)
+        spy_agency.spy_on(parse, call_fake=lambda _, log: ti)
         return ti
 
     return set_dag
diff --git a/task-sdk/src/airflow/sdk/execution_time/task_runner.py b/task-sdk/src/airflow/sdk/execution_time/task_runner.py
index 20bd5d271eb9d..a34a4c78ffa1a 100644
--- a/task-sdk/src/airflow/sdk/execution_time/task_runner.py
+++ b/task-sdk/src/airflow/sdk/execution_time/task_runner.py
@@ -535,7 +535,7 @@ def _xcom_push_to_db(ti: RuntimeTaskInstance, key: str, value: Any) -> None:
     )
 
 
-def parse(what: StartupDetails) -> RuntimeTaskInstance:
+def parse(what: StartupDetails, log: Logger) -> RuntimeTaskInstance:
     # TODO: Task-SDK:
     # Using DagBag here is about 98% wrong, but it'll do for now
 
@@ -558,12 +558,28 @@ def parse(what: StartupDetails) -> RuntimeTaskInstance:
     if TYPE_CHECKING:
         assert what.ti.dag_id
 
-    dag = bag.dags[what.ti.dag_id]
+    try:
+        dag = bag.dags[what.ti.dag_id]
+    except KeyError:
+        log.error(
+            "DAG not found during start up", dag_id=what.ti.dag_id, bundle=bundle_info, path=what.dag_rel_path
+        )
+        exit(1)
 
     # install_loader()
 
-    # TODO: Handle task not found
-    task = dag.task_dict[what.ti.task_id]
+    try:
+        task = dag.task_dict[what.ti.task_id]
+    except KeyError:
+        log.error(
+            "Task not found in DAG during start up",
+            dag_id=dag.dag_id,
+            task_id=what.ti.task_id,
+            bundle=bundle_info,
+            path=what.dag_rel_path,
+        )
+        exit(1)
+
     if not isinstance(task, (BaseOperator, MappedOperator)):
         raise TypeError(
             f"task is of the wrong type, got {type(task)}, wanted {BaseOperator} or {MappedOperator}"
@@ -674,7 +690,7 @@ def startup() -> tuple[RuntimeTaskInstance, Context, Logger]:
             setproctitle(f"airflow worker -- {msg.ti.id}")
 
         with _airflow_parsing_context_manager(dag_id=msg.ti.dag_id, task_id=msg.ti.task_id):
-            ti = parse(msg)
+            ti = parse(msg, log)
         log.debug("DAG file parsed", file=msg.dag_rel_path)
     else:
         raise RuntimeError(f"Unhandled startup message {type(msg)} {msg}")
diff --git a/task-sdk/tests/task_sdk/execution_time/test_task_runner.py b/task-sdk/tests/task_sdk/execution_time/test_task_runner.py
index 1b795180f94bf..29a1738c0a990 100644
--- a/task-sdk/tests/task_sdk/execution_time/test_task_runner.py
+++ b/task-sdk/tests/task_sdk/execution_time/test_task_runner.py
@@ -209,7 +209,7 @@ def test_parse(test_dags_dir: Path, make_ti_context):
             ),
         },
     ):
-        ti = parse(what)
+        ti = parse(what, mock.Mock())
 
     assert ti.task
     assert ti.task.dag
@@ -217,6 +217,65 @@ def test_parse(test_dags_dir: Path, make_ti_context):
     assert isinstance(ti.task.dag, DAG)
 
 
+@pytest.mark.parametrize(
+    ("dag_id", "task_id", "expected_error"),
+    (
+        pytest.param(
+            "madeup_dag_id",
+            "a",
+            mock.call(mock.ANY, dag_id="madeup_dag_id", path="super_basic.py"),
+            id="dag-not-found",
+        ),
+        pytest.param(
+            "super_basic",
+            "no-such-task",
+            mock.call(mock.ANY, task_id="no-such-task", dag_id="super_basic", path="super_basic.py"),
+            id="task-not-found",
+        ),
+    ),
+)
+def test_parse_not_found(test_dags_dir: Path, make_ti_context, dag_id, task_id, expected_error):
+    """Check for nice error messages on dag not found."""
+    what = StartupDetails(
+        ti=TaskInstance(
+            id=uuid7(),
+            task_id=task_id,
+            dag_id=dag_id,
+            run_id="c",
+            try_number=1,
+        ),
+        dag_rel_path="super_basic.py",
+        bundle_info=BundleInfo(name="my-bundle", version=None),
+        requests_fd=0,
+        ti_context=make_ti_context(),
+        start_date=timezone.utcnow(),
+    )
+
+    log = mock.Mock()
+
+    with (
+        patch.dict(
+            os.environ,
+            {
+                "AIRFLOW__DAG_PROCESSOR__DAG_BUNDLE_CONFIG_LIST": json.dumps(
+                    [
+                        {
+                            "name": "my-bundle",
+                            "classpath": "airflow.dag_processing.bundles.local.LocalDagBundle",
+                            "kwargs": {"path": str(test_dags_dir), "refresh_interval": 1},
+                        }
+                    ]
+                ),
+            },
+        ),
+        pytest.raises(SystemExit),
+    ):
+        parse(what, log)
+
+    expected_error.kwargs["bundle"] = what.bundle_info
+    log.error.assert_has_calls([expected_error])
+
+
 def test_run_deferred_basic(time_machine, create_runtime_ti, mock_supervisor_comms):
     """Test that a task can transition to a deferred state."""
     from airflow.providers.standard.sensors.date_time import DateTimeSensorAsync