diff --git a/src/documents/tests/test_api_search.py b/src/documents/tests/test_api_search.py
index 230b3f513..196c6f227 100644
--- a/src/documents/tests/test_api_search.py
+++ b/src/documents/tests/test_api_search.py
@@ -801,6 +801,26 @@ class TestDocumentSearchApi(DirectoriesMixin, APITestCase):
         self.assertEqual(response.status_code, status.HTTP_400_BAD_REQUEST)
         self.assertIn("invalid-date", str(response.data["query"]))
 
+    def test_search_multiple_bad_fields_returns_all_messages(self) -> None:
+        """
+        GIVEN:
+            - One document added
+        WHEN:
+            - Query with multiple bad fields (e.g. invalid date and invalid number)
+        THEN:
+            - 400 Bad Request with error messages for every bad field,
+              so the user can fix them all in one round-trip
+        """
+        response = self.client.get(
+            "/api/documents/",
+            {"query": "created:notadate AND asn:notanumber"},
+        )
+        self.assertEqual(response.status_code, status.HTTP_400_BAD_REQUEST)
+        messages = response.data["query"]
+        self.assertEqual(len(messages), 2)
+        self.assertTrue(any("created" in m for m in messages))
+        self.assertTrue(any("asn" in m for m in messages))
+
     @override_settings(
         TIME_ZONE="UTC",
     )
diff --git a/src/documents/views.py b/src/documents/views.py
index 68f786b6b..6e3a11fbc 100644
--- a/src/documents/views.py
+++ b/src/documents/views.py
@@ -2610,10 +2610,17 @@ class UnifiedSearchViewSet(DocumentViewSet):
         except ValidationError:
             raise
         except SearchQueryError as e:
-            # User-fixable query error (e.g. an unparsable date): surface the
-            # specific message so the user can correct it, rather than a generic
-            # 400 or silently empty results.
-            raise ValidationError({"query": [str(e)]}) from e
+            # User-fixable query error(s) (e.g. unparsable dates/numbers):
+            # surface every offending field's message, not just the first,
+            # so the user can fix them all in one round-trip.
+            from documents.search import MultipleSearchQueryErrors
+
+            messages = (
+                [str(sub) for sub in e.errors]
+                if isinstance(e, MultipleSearchQueryErrors)
+                else [str(e)]
+            )
+            raise ValidationError({"query": messages}) from e
         except Exception as e:
             logger.warning(f"An error occurred listing search results: {e!s}")
             return HttpResponseBadRequest(