diff -u b/core/misc/ajax.js b/core/misc/ajax.js
--- b/core/misc/ajax.js
+++ b/core/misc/ajax.js
@@ -1041,12 +1041,28 @@
       // https://www.drupal.org/node/736066.
 
       var $responseDataWrapped = $('<div></div>').html(response.data);
-      var $new_content = $responseDataWrapped.contents()
-        .filter(function (index, value) {
-          return value.nodeType === 1;
-        }).length === 1 && $responseDataWrapped.contents().length === 1 ?
-          $responseDataWrapped.children() :
-          $('<div></div>').html(response.data);
+      var $new_content = $('<div></div>');
+
+      var createWrapper = function () {
+        return $('<div></div>');
+      };
+
+      var wrapper = null;
+      $responseDataWrapped.contents().each(function (index, value) {
+        if (wrapper && value.nodeType !== 1) {
+          wrapper.append(value);
+        }
+        if (!wrapper && value.nodeType !== 1) {
+          wrapper = createWrapper();
+          wrapper.append(value);
+        }
+        if (wrapper && value.nodeType === 1) {
+          $new_content.append(wrapper, value);
+          wrapper = null;
+        }
+      });
+
+      $new_content = $new_content.children();
 
       // If removing content from the wrapper, detach behaviors first.
       switch (method) {
diff -u b/core/modules/system/tests/modules/ajax_test/src/Controller/AjaxTestController.php b/core/modules/system/tests/modules/ajax_test/src/Controller/AjaxTestController.php
--- b/core/modules/system/tests/modules/ajax_test/src/Controller/AjaxTestController.php
+++ b/core/modules/system/tests/modules/ajax_test/src/Controller/AjaxTestController.php
@@ -63,13 +63,14 @@
         break;
 
       case 'mixed':
-        $markup = 'outside<div>inside</div>';
+        $markup = ' what? <!-- THEME DEBUG -->  a  some text<div class="cool-guy-class"><p>some more text</p></div> ok and now some more, <!-- THEME DEBUG --> <p>ok</p>';
         break;
     }
     $content = [
       '#title' => '<em>AJAX Dialog & contents</em>',
       'content' => [
-        '#markup' => $markup,
+        '#type' => 'inline_template',
+        '#template' => $markup,
       ],
     ];
 
diff -u b/core/tests/Drupal/FunctionalJavascriptTests/Ajax/AjaxTest.php b/core/tests/Drupal/FunctionalJavascriptTests/Ajax/AjaxTest.php
--- b/core/tests/Drupal/FunctionalJavascriptTests/Ajax/AjaxTest.php
+++ b/core/tests/Drupal/FunctionalJavascriptTests/Ajax/AjaxTest.php
@@ -104,7 +104,7 @@
     $this->clickLink('Link 3 (mixed)');
     $assert->assertWaitOnAjaxRequest();
     $assert->responseContains('not-wrapped');
-    $assert->responseContains('<div>outside<div>inside</div></div>');
+    $assert->responseContains('what<b>what</b>');
 
   }