diff --git a/lib/galaxy/app.py b/lib/galaxy/app.py
index affa3ea7c85..0d7f1abc422 100644
--- a/lib/galaxy/app.py
+++ b/lib/galaxy/app.py
@@ -703,9 +703,6 @@ class UniverseApplication(StructuredApp, GalaxyManagerApplication):
         self.datatypes_registry.load_external_metadata_tool(self.toolbox)
         # Load history import/export tools.
         load_lib_tools(self.toolbox)
-        # Load built-in converters
-        if self.config.display_builtin_converters:
-            self.toolbox.load_builtin_converters()
         self.toolbox.persist_cache(register_postfork=True)
         # visualizations registry: associates resources with visualizations, controls how to render
         self.visualizations_registry = self._register_singleton(
diff --git a/lib/galaxy/app_unittest_utils/galaxy_mock.py b/lib/galaxy/app_unittest_utils/galaxy_mock.py
index d6a773e214e..9a9e21cbddc 100644
--- a/lib/galaxy/app_unittest_utils/galaxy_mock.py
+++ b/lib/galaxy/app_unittest_utils/galaxy_mock.py
@@ -158,6 +158,10 @@ class MockApp(di.Container, GalaxyDataTestApp):
     def toolbox(self) -> ToolBox:
         return self._toolbox
 
+    @toolbox.setter
+    def toolbox(self, toolbox: ToolBox):
+        self._toolbox = toolbox
+
     def wait_for_toolbox_reload(self, toolbox):
         # TODO: If the tpm test case passes, does the operation really
         # need to wait.
@@ -258,6 +262,7 @@ class MockAppConfig(GalaxyDataTestConfig, CommonConfigurationMixin):
         self.integrated_tool_panel_config = None
         self.vault_config_file = kwargs.get("vault_config_file")
         self.max_discovered_files = 10000
+        self.display_builtin_converters = True
         self.enable_notification_system = True
 
     @property
diff --git a/lib/galaxy/app_unittest_utils/tools_support.py b/lib/galaxy/app_unittest_utils/tools_support.py
index 6c94d5eb59d..e29b96dc029 100644
--- a/lib/galaxy/app_unittest_utils/tools_support.py
+++ b/lib/galaxy/app_unittest_utils/tools_support.py
@@ -1,6 +1,6 @@
 """ Module contains test fixtures meant to aide in the testing of jobs and
 tool evaluation. Such extensive "fixtures" are something of an anti-pattern
-so use of this should be limitted to tests of very 'extensive' classes.
+so use of this should be limited to tests of very 'extensive' classes.
 """
 
 import os.path
diff --git a/lib/galaxy/tools/__init__.py b/lib/galaxy/tools/__init__.py
index d94f5b4d3c0..5831359a841 100644
--- a/lib/galaxy/tools/__init__.py
+++ b/lib/galaxy/tools/__init__.py
@@ -442,7 +442,9 @@ class ToolBox(AbstractToolBox):
             default_panel_view=default_panel_view,
             save_integrated_tool_panel=save_integrated_tool_panel,
         )
-
+        # Load built-in converters
+        if app.config.display_builtin_converters:
+            self.load_builtin_converters()
         if old_toolbox := getattr(app, "toolbox", None):
             self.dependency_manager = old_toolbox.dependency_manager
         else:
diff --git a/test/unit/app/tools/test_toolbox.py b/test/unit/app/tools/test_toolbox.py
index f003fb51927..f4faaa370a1 100644
--- a/test/unit/app/tools/test_toolbox.py
+++ b/test/unit/app/tools/test_toolbox.py
@@ -239,13 +239,14 @@ class TestToolBox(BaseToolBoxTestCase):
         self.__verify_two_test_tools()
 
         # Assert tools merged in tool panel.
-        assert len(self.toolbox._tool_panel) == 1
+        assert len(self.toolbox._tool_panel) == 2  # 1 tool (w 2 versions) + built-in converters
 
     def test_get_section_by_label(self):
         self._add_config(
             """<toolbox><section id="tid" name="Completely unrelated"><label id="lab1" text="Label 1" /><label id="lab2" text="Label 2" /></section></toolbox>"""
         )
-        assert len(self.toolbox._tool_panel) == 1
+        print(self.toolbox._tool_panel)
+        assert len(self.toolbox._tool_panel) == 2  # section + built-in converters
         section = self.toolbox._tool_panel["tid"]
         tool_panel_section_key, section_by_label = self.toolbox.get_section(
             section_id="nope", new_label="Completely unrelated", create_if_needed=True
@@ -292,7 +293,7 @@ class TestToolBox(BaseToolBoxTestCase):
         stored_workflow = self.__test_workflow()
         encoded_id = self.app.security.encode_id(stored_workflow.id)
         self._add_config(f"""<toolbox><workflow id="{encoded_id}" /></toolbox>""")
-        assert len(self.toolbox._tool_panel) == 1
+        assert len(self.toolbox._tool_panel) == 2  # workflow + built-in converters section
         panel_workflow = next(iter(self.toolbox._tool_panel.values()))
         assert panel_workflow == stored_workflow.latest_workflow
         # TODO: test to_dict with workflows
@@ -303,7 +304,7 @@ class TestToolBox(BaseToolBoxTestCase):
         self._add_config(
             f"""<toolbox><section id="tid" name="TID"><workflow id="{encoded_id}" /></section></toolbox>"""
         )
-        assert len(self.toolbox._tool_panel) == 1
+        assert len(self.toolbox._tool_panel) == 2  # workflow + built-in converters section
         section = self.toolbox._tool_panel["tid"]
         assert len(section.elems) == 1
         panel_workflow = next(iter(section.elems.values()))
@@ -311,14 +312,14 @@ class TestToolBox(BaseToolBoxTestCase):
 
     def test_label_in_panel(self):
         self._add_config("""<toolbox><label id="lab1" text="Label 1" /><label id="lab2" text="Label 2" /></toolbox>""")
-        assert len(self.toolbox._tool_panel) == 2
+        assert len(self.toolbox._tool_panel) == 3  # 2 labels + built-in converters section
         self.__check_test_labels(self.toolbox._tool_panel)
 
     def test_label_in_section(self):
         self._add_config(
             """<toolbox><section id="tid" name="TID"><label id="lab1" text="Label 1" /><label id="lab2" text="Label 2" /></section></toolbox>"""
         )
-        assert len(self.toolbox._tool_panel) == 1
+        assert len(self.toolbox._tool_panel) == 2  # section + built-in converters section
         section = self.toolbox._tool_panel["tid"]
         self.__check_test_labels(section.elems)
 
@@ -336,7 +337,12 @@ class TestToolBox(BaseToolBoxTestCase):
             self._add_config({"items": [section]}, name="tool_conf.json")
 
     def __check_test_labels(self, panel_dict):
-        assert list(panel_dict.keys()) == ["label_lab1", "label_lab2"]
+        # if panel_dict is the complete panel it will contain builtin_converters
+        # if its a section then not
+        assert list(panel_dict.keys()) in (
+            ["label_lab1", "label_lab2", "builtin_converters"],
+            ["label_lab1", "label_lab2"],
+        )
         label1 = next(iter(panel_dict.values()))
         assert label1.id == "lab1"
         assert label1.text == "Label 1"
@@ -412,7 +418,7 @@ class TestToolBox(BaseToolBoxTestCase):
         self._init_tool(filename="tool_v02.xml", version="0.2")
 
     def __verify_tool_panel_for_default_lineage(self):
-        assert len(self.toolbox._tool_panel) == 1
+        assert len(self.toolbox._tool_panel) == 2  # tool + built-in-converters section
         tool = self.toolbox._tool_panel["tool_test_tool"]
         assert tool.version == "0.2", tool.version
         assert tool.id == "test_tool"
diff --git a/test/unit/tool_shed/test_tool_panel_manager.py b/test/unit/tool_shed/test_tool_panel_manager.py
index 751a7c5f5c4..9217b7347c6 100644
--- a/test/unit/tool_shed/test_tool_panel_manager.py
+++ b/test/unit/tool_shed/test_tool_panel_manager.py
@@ -25,20 +25,20 @@ class TestToolPanelManager(BaseToolBoxTestCase):
         assert section_id == "tid"
         assert len(section.elems) == 1  # tool.xml
         assert section.id == "tid"
-        assert len(toolbox._tool_panel) == 1
+        assert len(toolbox._tool_panel) == 2  # section + built-in converters section
 
         section_id, section = tpm.handle_tool_panel_section(toolbox, new_tool_panel_section_label="tid2")
         assert section_id == "tid2"
         assert len(section.elems) == 0  # new section
         assert section.id == "tid2"
-        assert len(toolbox._tool_panel) == 2
+        assert len(toolbox._tool_panel) == 3  # 2 sections + built-in converters section
 
         # Test re-fetch new section by same id.
         section_id, section = tpm.handle_tool_panel_section(toolbox, new_tool_panel_section_label="tid2")
         assert section_id == "tid2"
         assert len(section.elems) == 0  # new section
         assert section.id == "tid2"
-        assert len(toolbox._tool_panel) == 2
+        assert len(toolbox._tool_panel) == 3  # 2 sections + built-in converters section
 
     def test_add_tool_to_panel(self):
         self._init_ts_tool(guid=DEFAULT_GUID)