diff --git a/airflow-core/src/airflow/api_fastapi/execution_api/routes/dag_runs.py b/airflow-core/src/airflow/api_fastapi/execution_api/routes/dag_runs.py
index 2b178e97fc220..966a13d8dc817 100644
--- a/airflow-core/src/airflow/api_fastapi/execution_api/routes/dag_runs.py
+++ b/airflow-core/src/airflow/api_fastapi/execution_api/routes/dag_runs.py
@@ -153,6 +153,14 @@ def trigger_dag_run(
                 "message": f"A run already exists for Dag '{dag_id}' with run_id '{run_id}'",
             },
         )
+    except ValueError as e:
+        raise HTTPException(
+            status.HTTP_400_BAD_REQUEST,
+            detail={
+                "reason": "value_error",
+                "message": str(e),
+            },
+        ) from e
 
 
 @router.post(
diff --git a/airflow-core/tests/unit/api_fastapi/execution_api/versions/head/test_dag_runs.py b/airflow-core/tests/unit/api_fastapi/execution_api/versions/head/test_dag_runs.py
index 337bc1c90b8d5..31be920bd25fe 100644
--- a/airflow-core/tests/unit/api_fastapi/execution_api/versions/head/test_dag_runs.py
+++ b/airflow-core/tests/unit/api_fastapi/execution_api/versions/head/test_dag_runs.py
@@ -17,6 +17,8 @@
 
 from __future__ import annotations
 
+import re
+
 import pytest
 import time_machine
 from fastapi import Request
@@ -260,6 +262,31 @@ async def auth_as_parent_ti(request: Request) -> TIToken:
         child_run = session.scalars(select(DagRun).where(DagRun.run_id == child_run_id)).one()
         assert child_run.triggering_user_name == parent_triggering_user_name
 
+    def test_trigger_dag_run_value_error(self, client, session, dag_maker):
+        """Test that error is raised when a DAG Run has ValueError."""
+
+        dag_id = "test_trigger_dag_run_value_error"
+        run_id = "manual__{test_run_id}"
+        logical_date = timezone.datetime(2026, 5, 22)
+
+        with dag_maker(dag_id=dag_id, session=session, serialized=True):
+            EmptyOperator(task_id="test_task")
+
+        session.commit()
+
+        response = client.post(
+            f"/execution/dag-runs/{dag_id}/{run_id}",
+            json={"logical_date": logical_date.isoformat()},
+        )
+
+        detail_message = response.json()["detail"]["message"]
+        detail_reason = response.json()["detail"]["reason"]
+
+        pattern = r"The run_id provided '.*' does not match regex pattern '.*' or '.*'"
+        assert re.search(pattern, detail_message)
+        assert detail_reason == "value_error"
+        assert response.status_code == 400
+
 
 class TestDagRunClear:
     def setup_method(self):