diff --git a/django/contrib/admin/static/admin/js/admin/RelatedObjectLookups.js b/django/contrib/admin/static/admin/js/admin/RelatedObjectLookups.js
index 5c9c0d833d..752dcad7bf 100644
--- a/django/contrib/admin/static/admin/js/admin/RelatedObjectLookups.js
+++ b/django/contrib/admin/static/admin/js/admin/RelatedObjectLookups.js
@@ -96,7 +96,8 @@
         // Extract the model from the popup url '.../<model>/add/' or
         // '.../<model>/<id>/change/' depending the action (add or change).
         const modelName = path.split('/')[path.split('/').length - (objId ? 4 : 3)];
-        const selectsRelated = document.querySelectorAll(`[data-model-ref="${modelName}"] select`);
+        // Exclude autocomplete selects.
+        const selectsRelated = document.querySelectorAll(`[data-model-ref="${modelName}"] select:not(.admin-autocomplete)`);
 
         selectsRelated.forEach(function(select) {
             if (currentSelect === select) {
diff --git a/docs/releases/4.1.2.txt b/docs/releases/4.1.2.txt
index 6a473c16eb..809d583a78 100644
--- a/docs/releases/4.1.2.txt
+++ b/docs/releases/4.1.2.txt
@@ -23,3 +23,7 @@ Bugfixes
 * Fixed a regression in Django 4.1 that caused a
   ``QuerySet.values()/values_list()`` crash on ``ArrayAgg()`` and
   ``JSONBAgg()`` (:ticket:`34016`).
+
+* Fixed a bug in Django 4.1 that caused :attr:`.ModelAdmin.autocomplete_fields`
+  to be incorrectly selected after adding/changing related instances via popups
+  (:ticket:`34025`).
diff --git a/tests/admin_views/admin.py b/tests/admin_views/admin.py
index 996f7d5afc..9241034ffb 100644
--- a/tests/admin_views/admin.py
+++ b/tests/admin_views/admin.py
@@ -1165,6 +1165,14 @@ class GetFormsetsArgumentCheckingAdmin(admin.ModelAdmin):
         return super().get_formsets_with_inlines(request, obj)
 
 
+class CountryAdmin(admin.ModelAdmin):
+    search_fields = ["name"]
+
+
+class TravelerAdmin(admin.ModelAdmin):
+    autocomplete_fields = ["living_country"]
+
+
 site = admin.AdminSite(name="admin")
 site.site_url = "/my-site-url/"
 site.register(Article, ArticleAdmin)
@@ -1286,8 +1294,8 @@ site.register(ExplicitlyProvidedPK, GetFormsetsArgumentCheckingAdmin)
 site.register(ImplicitlyGeneratedPK, GetFormsetsArgumentCheckingAdmin)
 site.register(UserProxy)
 site.register(Box)
-site.register(Country)
-site.register(Traveler)
+site.register(Country, CountryAdmin)
+site.register(Traveler, TravelerAdmin)
 
 # Register core models we need in our tests
 site.register(User, UserAdmin)
diff --git a/tests/admin_views/tests.py b/tests/admin_views/tests.py
index 30010707d9..cd5b8ed836 100644
--- a/tests/admin_views/tests.py
+++ b/tests/admin_views/tests.py
@@ -6317,18 +6317,24 @@ class SeleniumTests(AdminSeleniumTestCase):
         finally:
             self.selenium.set_window_size(current_size["width"], current_size["height"])
 
-    def test_updating_related_objects_updates_fk_selects(self):
+    def test_updating_related_objects_updates_fk_selects_except_autocompletes(self):
         from selenium.webdriver.common.by import By
         from selenium.webdriver.support.ui import Select
 
         born_country_select_id = "id_born_country"
         living_country_select_id = "id_living_country"
+        living_country_select2_textbox_id = "select2-id_living_country-container"
         favorite_country_to_vacation_select_id = "id_favorite_country_to_vacation"
         continent_select_id = "id_continent"
 
         def _get_HTML_inside_element_by_id(id_):
             return self.selenium.find_element(By.ID, id_).get_attribute("innerHTML")
 
+        def _get_text_inside_element_by_selector(selector):
+            return self.selenium.find_element(By.CSS_SELECTOR, selector).get_attribute(
+                "innerText"
+            )
+
         self.admin_login(
             username="super", password="secret", login_url=reverse("admin:index")
         )
@@ -6353,12 +6359,16 @@ class SeleniumTests(AdminSeleniumTestCase):
             <option value="1" selected="">Argentina</option>
             """,
         )
-        self.assertHTMLEqual(
-            _get_HTML_inside_element_by_id(living_country_select_id),
-            """
-            <option value="" selected="">---------</option>
-            <option value="1">Argentina</option>
-            """,
+        # Argentina isn't added to the living_country select nor selected by
+        # the select2 widget.
+        self.assertEqual(
+            _get_text_inside_element_by_selector(f"#{living_country_select_id}"), ""
+        )
+        self.assertEqual(
+            _get_text_inside_element_by_selector(
+                f"#{living_country_select2_textbox_id}"
+            ),
+            "",
         )
         # Argentina won't appear because favorite_country_to_vacation field has
         # limit_choices_to.
@@ -6386,13 +6396,18 @@ class SeleniumTests(AdminSeleniumTestCase):
             <option value="2">Spain</option>
             """,
         )
-        self.assertHTMLEqual(
-            _get_HTML_inside_element_by_id(living_country_select_id),
-            """
-            <option value="" selected="">---------</option>
-            <option value="1">Argentina</option>
-            <option value="2" selected="">Spain</option>
-            """,
+
+        # Spain is added to the living_country select and it's also selected by
+        # the select2 widget.
+        self.assertEqual(
+            _get_text_inside_element_by_selector(f"#{living_country_select_id} option"),
+            "Spain",
+        )
+        self.assertEqual(
+            _get_text_inside_element_by_selector(
+                f"#{living_country_select2_textbox_id}"
+            ),
+            "Spain",
         )
         # Spain won't appear because favorite_country_to_vacation field has
         # limit_choices_to.
@@ -6422,13 +6437,17 @@ class SeleniumTests(AdminSeleniumTestCase):
             <option value="2">Italy</option>
             """,
         )
-        self.assertHTMLEqual(
-            _get_HTML_inside_element_by_id(living_country_select_id),
-            """
-            <option value="" selected="">---------</option>
-            <option value="1">Argentina</option>
-            <option value="2" selected="">Italy</option>
-            """,
+        # Italy is added to the living_country select and it's also selected by
+        # the select2 widget.
+        self.assertEqual(
+            _get_text_inside_element_by_selector(f"#{living_country_select_id} option"),
+            "Italy",
+        )
+        self.assertEqual(
+            _get_text_inside_element_by_selector(
+                f"#{living_country_select2_textbox_id}"
+            ),
+            "Italy",
         )
         # favorite_country_to_vacation field has no options.
         self.assertHTMLEqual(