diff --git a/aws_lambda_powertools/event_handler/api_gateway.py b/aws_lambda_powertools/event_handler/api_gateway.py
index d5d7751f043..a323cf67d56 100644
--- a/aws_lambda_powertools/event_handler/api_gateway.py
+++ b/aws_lambda_powertools/event_handler/api_gateway.py
@@ -3343,22 +3343,13 @@ def _get_base_path(self) -> str:
         # ALB doesn't have a stage variable, so we just return an empty string
         return ""
 
-    # BedrockResponse is not used here but adding the same signature to keep strong typing
     @override
     def _to_response(self, result: dict | tuple | Response | BedrockResponse) -> Response | BedrockResponse:
         """Convert the route's result to a Response
 
         ALB requires a non-null body otherwise it converts as HTTP 5xx
-
-         3 main result types are supported:
-
-        - Dict[str, Any]: Rest api response with just the Dict to json stringify and content-type is set to
-          application/json
-        - Tuple[dict, int]: Same dict handling as above but with the option of including a status code
-        - Response: returned as is, and allows for more flexibility
         """
-
-        # NOTE: Minor override for early return on Response with null body for ALB
+        # ALB doesn't support null body - convert before building the final response
         if isinstance(result, Response) and result.body is None:
             logger.debug("ALB doesn't allow None responses; converting to empty string")
             result.body = ""
diff --git a/aws_lambda_powertools/event_handler/middlewares/openapi_validation.py b/aws_lambda_powertools/event_handler/middlewares/openapi_validation.py
index 05306b5ca8b..470a19e6c54 100644
--- a/aws_lambda_powertools/event_handler/middlewares/openapi_validation.py
+++ b/aws_lambda_powertools/event_handler/middlewares/openapi_validation.py
@@ -296,9 +296,13 @@ def _handle_response(self, *, route: Route, response: Response):
                 # JSON serialize the body without validation
                 response.body = jsonable_encoder(response.body, custom_serializer=self._validation_serializer)
         else:
+            # ALB resolver converts None body to "" to prevent ALB 5xx errors,
+            # but the validation should still see it as None.
+            response_content = None if response.body == "" and field.type_ in (None, type(None)) else response.body
+
             response.body = self._serialize_response_with_validation(
                 field=field,
-                response_content=response.body,
+                response_content=response_content,
                 has_route_custom_response_validation=route.custom_response_validation_http_code is not None,
             )
 
diff --git a/tests/functional/event_handler/_pydantic/test_openapi_validation_middleware.py b/tests/functional/event_handler/_pydantic/test_openapi_validation_middleware.py
index e7199adc9c5..0da092f8aea 100644
--- a/tests/functional/event_handler/_pydantic/test_openapi_validation_middleware.py
+++ b/tests/functional/event_handler/_pydantic/test_openapi_validation_middleware.py
@@ -4227,3 +4227,39 @@ def handler(session_id: Annotated[str, Cookie()]):
     assert result["statusCode"] == 200
     body = json.loads(result["body"])
     assert body["session_id"] == "lattice_v1_abc"
+
+
+def test_alb_response_none_body_with_validation(gw_event_alb):
+    # GIVEN an ALBResolver with validation enabled
+    app = ALBResolver(enable_validation=True)
+
+    gw_event_alb["path"] = "/no-content"
+    gw_event_alb["httpMethod"] = "DELETE"
+
+    # WHEN a handler returns Response with body=None and return type is None
+    @app.delete("/no-content")
+    def handler() -> None:
+        return Response(status_code=204, body=None)
+
+    # THEN the response should be 204 with empty body (not 422 validation error)
+    result = app(gw_event_alb, {})
+    assert result["statusCode"] == 204
+    assert result["body"] == ""
+
+
+def test_alb_response_typed_none_body_with_validation(gw_event_alb):
+    # GIVEN an ALBResolver with validation enabled
+    app = ALBResolver(enable_validation=True)
+
+    gw_event_alb["path"] = "/no-content"
+    gw_event_alb["httpMethod"] = "DELETE"
+
+    # WHEN a handler returns Response[None] with body=None
+    @app.delete("/no-content")
+    def handler() -> Response[None]:
+        return Response(status_code=204, body=None)
+
+    # THEN the response should be 204 with empty body (not 422 validation error)
+    result = app(gw_event_alb, {})
+    assert result["statusCode"] == 204
+    assert result["body"] == ""