diff --git a/core/modules/layout_builder/tests/src/FunctionalJavascript/LayoutBuilderTest.php b/core/modules/layout_builder/tests/src/FunctionalJavascript/LayoutBuilderTest.php
index 6dbe8eb924..748d0fbd5e 100644
--- a/core/modules/layout_builder/tests/src/FunctionalJavascript/LayoutBuilderTest.php
+++ b/core/modules/layout_builder/tests/src/FunctionalJavascript/LayoutBuilderTest.php
@@ -118,8 +118,7 @@ public function testLayoutBuilderUi() {
 
     $assert_session->linkExists('Powered by Drupal');
     $this->clickLink('Powered by Drupal');
-    $assert_session->assertWaitOnAjaxRequest();
-    $assert_session->elementExists('css', '#drupal-off-canvas');
+    $this->waitForOffCanvasForm('layout_builder_add_block');
 
     $page->fillField('settings[label]', 'This is the label');
     $page->checkField('settings[label_display]');
@@ -188,8 +187,7 @@ public function testLayoutBuilderUi() {
     $this->markCurrentPage();
 
     $this->clickContextualLink('.block-system-powered-by-block', 'Configure');
-    $assert_session->assertWaitOnAjaxRequest();
-    $assert_session->elementExists('css', '#drupal-off-canvas');
+    $this->waitForOffCanvasForm('layout_builder_update_block');
 
     $page->fillField('settings[label]', 'This is the new label');
     $page->pressButton('Update');
@@ -203,8 +201,7 @@ public function testLayoutBuilderUi() {
 
     // Remove a block.
     $this->clickContextualLink('.block-system-powered-by-block', 'Remove block');
-    $assert_session->assertWaitOnAjaxRequest();
-    $assert_session->elementExists('css', '#drupal-off-canvas');
+    $this->waitForOffCanvasForm('layout_builder_remove_block');
 
     $page->pressButton('Remove');
     $assert_session->assertWaitOnAjaxRequest();
@@ -229,8 +226,7 @@ public function testLayoutBuilderUi() {
 
     $assert_session->linkExists('My custom block');
     $this->clickLink('My custom block');
-    $assert_session->assertWaitOnAjaxRequest();
-
+    $this->waitForOffCanvasForm('layout_builder_add_block');
     $page->pressButton('Add Block');
     $assert_session->assertWaitOnAjaxRequest();
     $assert_session->pageTextContains('This is the block content');
@@ -238,15 +234,13 @@ public function testLayoutBuilderUi() {
     // Remove both sections.
     $assert_session->linkExists('Remove section');
     $this->clickLink('Remove section');
-    $assert_session->assertWaitOnAjaxRequest();
-
+    $this->waitForOffCanvasForm('layout_builder_remove_section');
     $page->pressButton('Remove');
     $assert_session->assertWaitOnAjaxRequest();
 
     $assert_session->linkExists('Remove section');
     $this->clickLink('Remove section');
-    $assert_session->assertWaitOnAjaxRequest();
-
+    $this->waitForOffCanvasForm('layout_builder_remove_section');
     $page->pressButton('Remove');
     $assert_session->assertWaitOnAjaxRequest();
 
@@ -294,7 +288,7 @@ public function testConfigurableLayouts() {
 
     $assert_session->linkExists('Layout plugin (with settings)');
     $this->clickLink('Layout plugin (with settings)');
-    $assert_session->assertWaitOnAjaxRequest();
+    $this->waitForOffCanvasForm('layout_builder_configure_section');
     $assert_session->fieldExists('layout_settings[setting_1]');
     $page->pressButton('Add section');
     $assert_session->assertWaitOnAjaxRequest();
@@ -306,7 +300,7 @@ public function testConfigurableLayouts() {
     // Configure the existing section.
     $assert_session->linkExists('Configure section');
     $this->clickLink('Configure section');
-    $assert_session->assertWaitOnAjaxRequest();
+    $this->waitForOffCanvasForm('layout_builder_configure_section');
     $page->fillField('layout_settings[setting_1]', 'Test setting value');
     $page->pressButton('Update');
     $assert_session->assertWaitOnAjaxRequest();
@@ -374,8 +368,8 @@ protected function clickContextualLink($selector, $link_locator, $force_visible
     $assert_session = $this->assertSession();
 
     if ($force_visible) {
-      $this->getSession()->executeScript("jQuery('{$selector} .contextual .trigger').removeClass('visually-hidden');");
-      $assert_session->assertWaitOnAjaxRequest();
+      $this->getSession()->executeScript("jQuery('{$selector} .contextual button').removeClass('visually-hidden');");
+      $assert_session->waitForElementVisible('css', '.contextual button');
     }
 
     $element = $this->getSession()->getPage()->find('css', $selector);
@@ -387,7 +381,7 @@ protected function clickContextualLink($selector, $link_locator, $force_visible
       // If the link is not visible, click the contextual link button first.
       if (!$link->isVisible()) {
         $element->find('css', '.contextual button')->press();
-        $assert_session->assertWaitOnAjaxRequest();
+        $assert_session->waitForLink($link_locator);
       }
       $this->assertTrue($link->isVisible(), "Link $link_locator is visible.");
       $link->click();
@@ -399,4 +393,33 @@ protected function clickContextualLink($selector, $link_locator, $force_visible
     }
   }
 
+  /**
+   * Waits for the specified form and returns it when available and visible.
+   *
+   * @param string $expected_form_id
+   *   The expected form ID.
+   * @param int $timeout
+   *   (Optional) Timeout in milliseconds, defaults to 10000.
+   *
+   * @return \Behat\Mink\Element\NodeElement|null
+   *   The form element if found and visible, NULL if not.
+   */
+  protected function waitForOffCanvasForm($expected_form_id, $timeout = 10000) {
+    $page = $this->getSession()->getPage();
+    return $page->waitFor($timeout / 1000, function () use ($page, $expected_form_id) {
+      // Ensure the form ID exists, is visible, and has the correct value.
+      $form_id_element = $page->find('hidden_field_selector', ['hidden_field', 'form_id']);
+      if (!$form_id_element || !$form_id_element->isVisible() || $expected_form_id !== $form_id_element->getValue()) {
+        return NULL;
+      }
+
+      // Ensure the off canvas dialog is visible.
+      $off_canvas = $page->find('css', '#drupal-off-canvas');
+      if (!$off_canvas || !$off_canvas->isVisible()) {
+        return NULL;
+      }
+      return $form_id_element;
+    });
+  }
+
 }