diff --git a/scripts/modules/addon_utils.py b/scripts/modules/addon_utils.py
index f4edb440e80..928f17ba236 100644
--- a/scripts/modules/addon_utils.py
+++ b/scripts/modules/addon_utils.py
@@ -536,8 +536,9 @@ def reset_all(*, reload_scripts=False):
     """
     import sys
 
-    # initializes addons_fake_modules
-    modules_refresh()
+    # Ensures stale `addons_fake_modules` isn't used.
+    modules._is_first = True
+    addons_fake_modules.clear()
 
     for path, pkg_id in _paths_with_extension_repos():
         if not pkg_id:
diff --git a/scripts/startup/bl_operators/userpref.py b/scripts/startup/bl_operators/userpref.py
index 8c4837d2736..42bb822e7d9 100644
--- a/scripts/startup/bl_operators/userpref.py
+++ b/scripts/startup/bl_operators/userpref.py
@@ -852,6 +852,8 @@ class PREFERENCES_OT_addon_expand(Operator):
 
         addon_module_name = self.module
 
+        # Ensure `addons_fake_modules` is set.
+        _modules = addon_utils.modules(refresh=False)
         mod = addon_utils.addons_fake_modules.get(addon_module_name)
         if mod is not None:
             bl_info = addon_utils.module_bl_info(mod)
@@ -876,6 +878,7 @@ class PREFERENCES_OT_addon_show(Operator):
 
         addon_module_name = self.module
 
+        # Ensure `addons_fake_modules` is set.
         _modules = addon_utils.modules(refresh=False)
         mod = addon_utils.addons_fake_modules.get(addon_module_name)
         if mod is not None:
diff --git a/source/blender/windowmanager/intern/wm_files.cc b/source/blender/windowmanager/intern/wm_files.cc
index bd6daebd385..1ccf2dcaeb9 100644
--- a/source/blender/windowmanager/intern/wm_files.cc
+++ b/source/blender/windowmanager/intern/wm_files.cc
@@ -671,6 +671,7 @@ struct wmFileReadPost_Params {
   /* Used by #wm_homefile_read_post. */
   uint success : 1;
   uint is_alloc : 1;
+  uint is_first_time : 1;
 };
 
 /**
@@ -701,11 +702,10 @@ static void wm_file_read_post(bContext *C,
 
 #ifdef WITH_PYTHON
   if (is_startup_file) {
-    /* On startup (by default), Python won't have been initialized.
-     *
-     * The following block handles data & preferences being reloaded
+    /* The following block handles data & preferences being reloaded
      * which requires resetting some internal variables. */
-    if (CTX_py_init_get(C)) {
+    if (!params->is_first_time) {
+      BLI_assert(CTX_py_init_get(C));
       bool reset_all = use_userdef;
       if (use_userdef || reset_app_template) {
         /* Only run when we have a template path found. */
@@ -1249,7 +1249,8 @@ void wm_homefile_read_ex(bContext *C,
   if (use_userdef || reset_app_template) {
 #ifdef WITH_PYTHON
     /* This only runs once Blender has already started. */
-    if (CTX_py_init_get(C)) {
+    if (!params_homefile->is_first_time) {
+      BLI_assert(CTX_py_init_get(C));
       /* This is restored by 'wm_file_read_post', disable before loading any preferences
        * so an add-on can read their own preferences when un-registering,
        * and use new preferences if/when re-registering, see #67577.
@@ -1502,6 +1503,8 @@ void wm_homefile_read_ex(bContext *C,
     params_file_read_post.use_userdef = use_userdef;
     params_file_read_post.is_startup_file = true;
     params_file_read_post.is_factory_startup = is_factory_startup;
+    params_file_read_post.is_first_time = params_homefile->is_first_time;
+
     params_file_read_post.reset_app_template = reset_app_template;
 
     params_file_read_post.success = success;
diff --git a/source/blender/windowmanager/intern/wm_init_exit.cc b/source/blender/windowmanager/intern/wm_init_exit.cc
index d675461490b..4eff54aa44a 100644
--- a/source/blender/windowmanager/intern/wm_init_exit.cc
+++ b/source/blender/windowmanager/intern/wm_init_exit.cc
@@ -276,6 +276,7 @@ void WM_init(bContext *C, int argc, const char **argv)
   read_homefile_params.use_empty_data = false;
   read_homefile_params.filepath_startup_override = nullptr;
   read_homefile_params.app_template_override = WM_init_state_app_template_get();
+  read_homefile_params.is_first_time = true;
 
   wm_homefile_read_ex(C, &read_homefile_params, nullptr, &params_file_read_post);
 
diff --git a/source/blender/windowmanager/wm_files.hh b/source/blender/windowmanager/wm_files.hh
index c365b7c4ba1..54e784041f7 100644
--- a/source/blender/windowmanager/wm_files.hh
+++ b/source/blender/windowmanager/wm_files.hh
@@ -42,6 +42,11 @@ struct wmHomeFileRead_Params {
    * Useful for automated content generation, so the file starts without data.
    */
   unsigned int use_empty_data : 1;
+  /**
+   * When true, this is the first time the home file is read.
+   * In this case resetting the previous state can be skipped.
+   */
+  unsigned int is_first_time : 1;
   /**
    * Optional path pointing to an alternative blend file (may be NULL).
    */