diff --git a/backend/open_webui/internal/db.py b/backend/open_webui/internal/db.py
index a7326aeafc..e0d9c9ede6 100644
--- a/backend/open_webui/internal/db.py
+++ b/backend/open_webui/internal/db.py
@@ -232,6 +232,27 @@ def _make_async_url(url: str) -> str:
     return url
 
 
+def _json_codec_kwargs(kwargs: dict) -> dict:
+    """Default an engine to JSONCodec for native ``JSON`` columns.
+
+    Unlike ``JSONField``, those serialize through the engine, which otherwise uses
+    stdlib ``json``. With ``ENABLE_ORJSON`` off JSONCodec is stdlib ``json`` anyway.
+    """
+    kwargs.setdefault('json_serializer', JSONCodec.dumps)
+    kwargs.setdefault('json_deserializer', JSONCodec.loads)
+    return kwargs
+
+
+def _create_engine(*args, **kwargs):
+    """``create_engine`` with the app JSON codec wired in."""
+    return create_engine(*args, **_json_codec_kwargs(kwargs))
+
+
+def _create_async_engine(*args, **kwargs):
+    """``create_async_engine`` with the app JSON codec wired in."""
+    return create_async_engine(*args, **_json_codec_kwargs(kwargs))
+
+
 # ============================================================
 # SYNC ENGINE (used only for: startup migrations, config loading,
 #              Alembic, peewee migration, health checks)
@@ -260,7 +281,7 @@ if SQLALCHEMY_DATABASE_URL.startswith('sqlite+sqlcipher://'):
     # in the native sqlcipher3 C library. Use NullPool by default for safety,
     # or QueuePool if DATABASE_POOL_SIZE is explicitly configured.
     if isinstance(DATABASE_POOL_SIZE, int) and DATABASE_POOL_SIZE > 0:
-        engine = create_engine(
+        engine = _create_engine(
             'sqlite://',
             creator=create_sqlcipher_connection,
             pool_size=DATABASE_POOL_SIZE,
@@ -272,7 +293,7 @@ if SQLALCHEMY_DATABASE_URL.startswith('sqlite+sqlcipher://'):
             echo=False,
         )
     else:
-        engine = create_engine(
+        engine = _create_engine(
             'sqlite://',
             creator=create_sqlcipher_connection,
             poolclass=NullPool,
@@ -282,7 +303,7 @@ if SQLALCHEMY_DATABASE_URL.startswith('sqlite+sqlcipher://'):
     log.info('Connected to encrypted SQLite database using SQLCipher')
 
 elif 'sqlite' in SQLALCHEMY_DATABASE_URL:
-    engine = create_engine(SQLALCHEMY_DATABASE_URL, connect_args={'check_same_thread': False})
+    engine = _create_engine(SQLALCHEMY_DATABASE_URL, connect_args={'check_same_thread': False})
 
     def _apply_sqlite_pragmas(dbapi_connection):
         """Apply all configured SQLite PRAGMAs to a raw DBAPI connection."""
@@ -314,7 +335,7 @@ elif 'sqlite' in SQLALCHEMY_DATABASE_URL:
 else:
     if isinstance(DATABASE_POOL_SIZE, int):
         if DATABASE_POOL_SIZE > 0:
-            engine = create_engine(
+            engine = _create_engine(
                 SQLALCHEMY_DATABASE_URL,
                 pool_size=DATABASE_POOL_SIZE,
                 max_overflow=DATABASE_POOL_MAX_OVERFLOW,
@@ -324,9 +345,9 @@ else:
                 poolclass=QueuePool,
             )
         else:
-            engine = create_engine(SQLALCHEMY_DATABASE_URL, pool_pre_ping=True, poolclass=NullPool)
+            engine = _create_engine(SQLALCHEMY_DATABASE_URL, pool_pre_ping=True, poolclass=NullPool)
     else:
-        engine = create_engine(SQLALCHEMY_DATABASE_URL, pool_pre_ping=True)
+        engine = _create_engine(SQLALCHEMY_DATABASE_URL, pool_pre_ping=True)
 
 enable_iam_token_auth(engine)
 
@@ -373,7 +394,7 @@ if 'sqlite' in ASYNC_SQLALCHEMY_DATABASE_URL:
     # No pool_pre_ping: a local SQLite file cannot drop connections, and the
     # ping costs a worker-thread hop plus a SELECT 1 on every checkout.
     _sqlite_pool_size = DATABASE_POOL_SIZE if isinstance(DATABASE_POOL_SIZE, int) and DATABASE_POOL_SIZE > 0 else 512
-    async_engine = create_async_engine(
+    async_engine = _create_async_engine(
         ASYNC_SQLALCHEMY_DATABASE_URL,
         connect_args={'check_same_thread': False},
         pool_size=_sqlite_pool_size,
@@ -387,7 +408,7 @@ if 'sqlite' in ASYNC_SQLALCHEMY_DATABASE_URL:
 else:
     if isinstance(DATABASE_POOL_SIZE, int):
         if DATABASE_POOL_SIZE > 0:
-            async_engine = create_async_engine(
+            async_engine = _create_async_engine(
                 ASYNC_SQLALCHEMY_DATABASE_URL,
                 pool_size=DATABASE_POOL_SIZE,
                 max_overflow=DATABASE_POOL_MAX_OVERFLOW,
@@ -396,13 +417,13 @@ else:
                 pool_pre_ping=True,
             )
         else:
-            async_engine = create_async_engine(
+            async_engine = _create_async_engine(
                 ASYNC_SQLALCHEMY_DATABASE_URL,
                 pool_pre_ping=True,
                 poolclass=NullPool,
             )
     else:
-        async_engine = create_async_engine(
+        async_engine = _create_async_engine(
             ASYNC_SQLALCHEMY_DATABASE_URL,
             pool_pre_ping=True,
         )