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 31d0831bbadec..6da2531febdad 100644
--- a/task-sdk/src/airflow/sdk/execution_time/task_runner.py
+++ b/task-sdk/src/airflow/sdk/execution_time/task_runner.py
@@ -1623,7 +1623,16 @@ def _on_term(signum, frame):
         msg, state = _handle_current_task_success(context, ti)
     except DagRunTriggerException as drte:
         log.info("::group::Post Execute")
-        msg, state = _handle_trigger_dag_run(drte, context, ti, log)
+        try:
+            msg, state = _handle_trigger_dag_run(drte, context, ti, log)
+        except (AirflowTaskTimeout, AirflowException, AirflowRuntimeError) as e:
+            # Errors returned by the API server (for example a 404 for a missing
+            # target DAG) are raised while handling the trigger exception. They
+            # must still use the normal failure path so retries and callbacks run.
+            log.exception("Task failed while triggering DagRun")
+            log.info("::group::Post Execute")
+            msg, state = _handle_current_task_failed(ti, e, log, context)
+            error = e
     except TaskDeferred as defer:
         log.info("::group::Post Execute")
         msg, state = _defer_task(defer, ti, log)
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 0031974b86646..da8db6a22bffd 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
@@ -5180,6 +5180,37 @@ def _send(msg=None, **kwargs):
         with pytest.raises(_TriggerSendError):
             run(ti, ti.get_template_context(), log)
 
+    @time_machine.travel("2025-01-01 00:00:00", tick=False)
+    def test_handle_trigger_dag_run_api_error_uses_failure_path(
+        self, create_runtime_ti, mock_supervisor_comms
+    ):
+        """API errors while triggering a DAG should honor the task retry policy."""
+        task = TriggerDagRunOperator(
+            task_id="test_task",
+            trigger_dag_id="missing_dag",
+            trigger_run_id="test_run_id",
+            retries=1,
+        )
+        ti = create_runtime_ti(
+            dag_id="test_handle_trigger_dag_run_api_error",
+            run_id="test_run",
+            task=task,
+            should_retry=True,
+        )
+
+        def _send(msg=None, **kwargs):
+            if isinstance(msg, TriggerDagRun):
+                raise AirflowRuntimeError("target DAG was not found")
+            return mock.DEFAULT
+
+        mock_supervisor_comms.send.side_effect = _send
+
+        state, msg, error = run(ti, ti.get_template_context(), mock.MagicMock())
+
+        assert state == TaskInstanceState.UP_FOR_RETRY
+        assert msg.state == TaskInstanceState.UP_FOR_RETRY
+        assert isinstance(error, AirflowRuntimeError)
+
     @pytest.mark.parametrize(
         ("allowed_states", "failed_states", "target_dr_state", "expected_task_state"),
         [