diff -u b/core/misc/ajax.js b/core/misc/ajax.js
--- b/core/misc/ajax.js
+++ b/core/misc/ajax.js
@@ -1042,26 +1042,37 @@
 
       var $responseDataWrapped = $('<div></div>').html(response.data);
       var $new_content = $('<div></div>');
+      var elementsReturned = $responseDataWrapped.contents().length;
 
       var createWrapper = function () {
         return $('<div></div>');
       };
 
-      var wrapper = null;
+      var intermediateWrapper = null;
       $responseDataWrapped.contents().each(function (index, value) {
-        if (wrapper && value.nodeType !== 1) {
-          wrapper.append(value);
+        if (intermediateWrapper && value.nodeType !== 1) {
+          intermediateWrapper.append(value);
         }
-        if (!wrapper && value.nodeType !== 1) {
-          wrapper = createWrapper();
-          wrapper.append(value);
+        if (!intermediateWrapper && value.nodeType !== 1) {
+          intermediateWrapper = createWrapper();
+          intermediateWrapper.append(value);
         }
-        if (wrapper && value.nodeType === 1) {
-          $new_content.append(wrapper, value);
-          wrapper = null;
+        if (!intermediateWrapper && value.nodeType === 1) {
+          $new_content.append(value);
+          intermediateWrapper = null;
+        }
+        if (intermediateWrapper && value.nodeType === 1) {
+          $new_content.append(intermediateWrapper, value);
+          intermediateWrapper = null;
         }
       });
 
+      // If we only had one element returned, and not an Node.ELEMENT_NODE
+      // we need to add it to $new_content
+      if (elementsReturned === 1) {
+        $new_content.append(intermediateWrapper);
+      }
+
       $new_content = $new_content.children();
 
       // If removing content from the wrapper, detach behaviors first.
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
@@ -55,7 +55,7 @@
     // This is a regular render array; the keys do not have special meaning.
     switch ($type) {
       case 'pre-wrapped':
-        $markup = '<div>wrapped</div>';
+        $markup = '<div class="pre-wrapped">pre-wrapped</div>';
         break;
 
       case 'not-wrapped':
@@ -63,7 +63,7 @@
         break;
 
       case 'mixed':
-        $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>';
+        $markup = ' foo <!-- COMMENT -->  foo bar<div class="a class"><p>some string</p></div> additional wrapped strings, <!-- ANOTHER COMMENT --> <p>final string</p>';
         break;
     }
     $content = [
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
@@ -92,7 +92,7 @@
     $this->drupalGet('ajax-test/insert');
     $this->clickLink('Link 1 (pre-wrapped)');
     $assert->assertWaitOnAjaxRequest();
-    $assert->responseContains('<div>wrapped</div>');
+    $assert->responseContains('<div class="pre-wrapped">pre-wrapped</div>');
 
     $this->drupalGet('ajax-test/insert');
     $this->clickLink('Link 2 (not wrapped)');
@@ -104,7 +104,7 @@
     $this->clickLink('Link 3 (mixed)');
     $assert->assertWaitOnAjaxRequest();
     $assert->responseContains('not-wrapped');
-    $assert->responseContains('what<b>what</b>');
+    $assert->responseContains('<div> foo <!-- COMMENT -->  foo bar</div><div class="a class"><p>some string</p></div><div> additional wrapped strings, <!-- ANOTHER COMMENT --> </div><p>final string</p>');
 
   }