diff --git a/datasette/views/table.py b/datasette/views/table.py
index 3e8f38f6..e6ae67de 100644
--- a/datasette/views/table.py
+++ b/datasette/views/table.py
@@ -915,6 +915,14 @@ class TableView(RowTableShared):
                         links.extend(extra_links)
                 return links
 
+            # filter_columns combine the columns we know are available
+            # in the table with any additional columns (such as rowid)
+            # which are available in the query
+            filter_columns = list(columns) + [
+                table_column
+                for table_column in table_columns
+                if table_column not in columns
+            ]
             return {
                 "table_actions": table_actions,
                 "supports_search": bool(fts_table),
@@ -922,7 +930,7 @@ class TableView(RowTableShared):
                 "use_rowid": use_rowid,
                 "filters": filters,
                 "display_columns": display_columns,
-                "filter_columns": table_columns,
+                "filter_columns": filter_columns,
                 "display_rows": display_rows,
                 "facets_timed_out": facets_timed_out,
                 "sorted_facet_results": sorted(
diff --git a/tests/test_html.py b/tests/test_html.py
index eb1e3d20..f24165bd 100644
--- a/tests/test_html.py
+++ b/tests/test_html.py
@@ -936,10 +936,11 @@ def test_table_html_filter_form_still_shows_nocol_columns(app_client):
         "pk1",
         "pk2",
         "content",
-        "sortable",
         "sortable_with_nulls",
         "sortable_with_nulls_2",
         "text",
+        # Moved to the end because it is no longer returned by the query:
+        "sortable",
     ]