diff --git a/src/Control/RequestHandler.php b/src/Control/RequestHandler.php
index 872c6a05b..6bee1a6b7 100644
--- a/src/Control/RequestHandler.php
+++ b/src/Control/RequestHandler.php
@@ -678,4 +678,15 @@ class RequestHandler extends ViewableData
         $url = Director::absoluteURL((string) $url);
         return $this->redirect($url);
     }
+
+    /**
+     * Convert an array of data to JSON and wrap it in an HTML tag as pjax is used and jQuery will parse this
+     * as an element on the client side in LeftAndMain.js handleAjaxResponse()
+     * The attribute type="application/json" denotes this is a data block and won't be processed by a browser
+     * https://html.spec.whatwg.org/#the-script-element
+     */
+    protected function prepareDataForPjax(array $data): string
+    {
+        return '<script type="application/json">' . json_encode($data) . '</script>';
+    }
 }
diff --git a/src/Forms/GridField/GridFieldDetailForm_ItemRequest.php b/src/Forms/GridField/GridFieldDetailForm_ItemRequest.php
index 150657207..f4294dd94 100644
--- a/src/Forms/GridField/GridFieldDetailForm_ItemRequest.php
+++ b/src/Forms/GridField/GridFieldDetailForm_ItemRequest.php
@@ -7,6 +7,7 @@ use SilverStripe\Admin\LeftAndMain;
 use SilverStripe\Control\Controller;
 use SilverStripe\Control\HTTPRequest;
 use SilverStripe\Control\HTTPResponse;
+use SilverStripe\Control\PjaxResponseNegotiator;
 use SilverStripe\Control\RequestHandler;
 use SilverStripe\Core\Convert;
 use SilverStripe\Core\ClassInfo;
@@ -170,7 +171,7 @@ class GridFieldDetailForm_ItemRequest extends RequestHandler
         ])->renderWith($this->getTemplates());
 
         if ($request->isAjax()) {
-            return $return;
+            return $this->getResponseNegotiator($return)->respond($request);
         } else {
             // If not requested by ajax, we need to render it within the controller context+template
             return $controller->customise([
@@ -298,6 +299,23 @@ class GridFieldDetailForm_ItemRequest extends RequestHandler
             }
 
             $form->Backlink = $this->getBackLink();
+
+            // Ensure the correct validation response is returned for AJAX requests
+            $form->setValidationResponseCallback(function (ValidationResult $errors) use ($form) {
+                $request = $this->getRequest();
+                if (!$request->isAjax()) {
+                    return null;
+                }
+                $negotiator = $this->getResponseNegotiator($form->forTemplate());
+                return $negotiator->respond($request, [
+                    'ValidationResult' => function () use ($errors) {
+                        return $this->prepareDataForPjax([
+                            'isValid' => $errors->isValid(),
+                            'messages' => $errors->getMessages()
+                        ]);
+                    }
+                ]);
+            });
         }
 
         $cb = $this->component->getItemEditFormCallback();
@@ -945,4 +963,36 @@ class GridFieldDetailForm_ItemRequest extends RequestHandler
         }
         return ClassInfo::shortName($this->record);
     }
+
+    /**
+     * Get Pjax response negotiator so form submission mirrors other form submission in the CMS.
+     * See LeftAndMain::getResponseNegotiator()
+     */
+    private function getResponseNegotiator(DBHTMLText $renderedForm): PjaxResponseNegotiator
+    {
+        return new PjaxResponseNegotiator([
+            'default' => function () use ($renderedForm) {
+                return $renderedForm;
+            },
+            'Content' => function () use ($renderedForm) {
+                return $renderedForm;
+            },
+            'CurrentForm' => function () use ($renderedForm) {
+                return $renderedForm;
+            },
+            'Breadcrumbs' => function () {
+                return $this->renderWith([
+                    'type' => 'Includes',
+                    'SilverStripe\\Admin\\CMSBreadcrumbs'
+                ]);
+            },
+            'ValidationResult' => function () {
+                // Assume valid by default, mirroring LeftAndMain's response negotiator
+                return $this->prepareDataForPjax([
+                    'isValid' => true,
+                    'messages' => '',
+                ]);
+            }
+        ], $this->getToplevelController()->getResponse());
+    }
 }