diff --git a/airflow-core/src/airflow/models/dagbag.py b/airflow-core/src/airflow/models/dagbag.py
index c4bd8eceea102..7dd748397cfd7 100644
--- a/airflow-core/src/airflow/models/dagbag.py
+++ b/airflow-core/src/airflow/models/dagbag.py
@@ -18,6 +18,7 @@
 from __future__ import annotations
 
 import hashlib
+import logging
 import time
 from collections.abc import MutableMapping
 from contextlib import nullcontext
@@ -43,6 +44,8 @@
     from airflow.models.serialized_dag import SerializedDagModel
     from airflow.serialization.definitions.dag import SerializedDAG
 
+log = logging.getLogger(__name__)
+
 
 class _CacheEntry(NamedTuple):
     """A cached deserialized DAG plus the metadata needed to detect staleness on lookup."""
@@ -104,7 +107,14 @@ def __init__(
     def _read_dag(self, serdag: SerializedDagModel) -> SerializedDAG | None:
         """Read and cache a SerializedDAG (with its ``dag_hash`` for staleness detection)."""
         serdag.load_op_links = self.load_op_links
-        dag = serdag.dag
+        try:
+            dag = serdag.dag
+        except Exception:
+            # A serialized blob that exists but cannot be reconstructed (unimportable operator class,
+            # incompatible serialization version, blob written under a synthetic bundle by
+            # dag.test()) is treated as "no live definition" so read-only callers return 404, not 500.
+            log.warning("Failed to deserialize DAG from %r; treating as not found", serdag, exc_info=True)
+            return None
         if not dag:
             return None
         with self._lock:
diff --git a/airflow-core/tests/unit/models/test_dagbag.py b/airflow-core/tests/unit/models/test_dagbag.py
index 79668d4fe54f4..1b9dd06e26e16 100644
--- a/airflow-core/tests/unit/models/test_dagbag.py
+++ b/airflow-core/tests/unit/models/test_dagbag.py
@@ -77,6 +77,26 @@ def test__read_dag_returns_none_when_no_dag(self):
         assert result is None
         assert "v1" not in self.db_dag_bag._dags
 
+    def test__read_dag_returns_none_when_deserialization_fails(self):
+        """A blob that exists but cannot be deserialized is treated as absent, not propagated.
+
+        Keeps read-only API callers (e.g. the DAG detail page) returning 404 instead of 500 for a
+        Dag whose serialized definition references an unimportable class or an incompatible version.
+        """
+
+        class _Undeserializable:
+            load_op_links = True
+            dag_version_id = "v1"
+
+            @property
+            def dag(self):
+                raise ValueError("cannot deserialize")
+
+        result = self.db_dag_bag._read_dag(_Undeserializable())
+
+        assert result is None
+        assert "v1" not in self.db_dag_bag._dags
+
     def test_get_dag_fetches_from_db_on_miss(self):
         """It should query the DB and cache the result (with its hash) when not in cache."""
         mock_dag = MagicMock(spec=SerializedDAG)