diff --git a/core/modules/layout_builder/tests/src/FunctionalJavascript/LayoutBuilderTest.php b/core/modules/layout_builder/tests/src/FunctionalJavascript/LayoutBuilderTest.php
index f98f80fb23f..fe995ec24b0 100644
--- a/core/modules/layout_builder/tests/src/FunctionalJavascript/LayoutBuilderTest.php
+++ b/core/modules/layout_builder/tests/src/FunctionalJavascript/LayoutBuilderTest.php
@@ -7,6 +7,7 @@ use Drupal\block_content\Entity\BlockContentType;
 use Drupal\Core\Url;
 use Drupal\FunctionalJavascriptTests\WebDriverTestBase;
 use Drupal\Tests\contextual\FunctionalJavascript\ContextualLinkClickTrait;
+use Drupal\Tests\system\Traits\OffCanvasTestTrait;
 
 /**
  * Tests the Layout Builder UI.
@@ -17,6 +18,7 @@ class LayoutBuilderTest extends WebDriverTestBase {
 
   use ContextualLinkClickTrait;
   use LayoutBuilderSortTrait;
+  use OffCanvasTestTrait;
 
   /**
    * {@inheritdoc}
@@ -27,6 +29,7 @@ class LayoutBuilderTest extends WebDriverTestBase {
     'layout_builder',
     'layout_test',
     'node',
+    'off_canvas_test',
   ];
 
   /**
@@ -285,17 +288,19 @@ class LayoutBuilderTest extends WebDriverTestBase {
     $assert_session->linkExists('Add section');
     $this->clickLink('Add section');
     $assert_session->assertWaitOnAjaxRequest();
-    $assert_session->elementExists('css', '#drupal-off-canvas');
+    $this->waitForOffCanvasArea();
 
     $assert_session->linkExists('One column');
     $this->clickLink('One column');
     $assert_session->assertWaitOnAjaxRequest();
+    $this->waitForOffCanvasArea();
 
     // Add another section.
     $assert_session->linkExists('Add section');
     $this->clickLink('Add section');
+
+    $this->waitForOffCanvasArea();
     $assert_session->waitForElementVisible('named', ['link', 'Layout plugin (with settings)']);
-    $assert_session->elementExists('css', '#drupal-off-canvas');
 
     $assert_session->linkExists('Layout plugin (with settings)');
     $this->clickLink('Layout plugin (with settings)');
@@ -310,9 +315,10 @@ class LayoutBuilderTest extends WebDriverTestBase {
     // Ensure validation error is displayed for ConfigureSectionForm.
     $assert_session->linkExists('Add section');
     $this->clickLink('Add section');
+    $this->waitForOffCanvasArea();
+
     $assert_session->waitForElementVisible('named', ['link', 'Layout plugin (with settings)']);
     $this->clickLink('Layout plugin (with settings)');
-    $this->markTestSkipped('Temporarily skipped due to random failures.');
     $this->assertOffCanvasFormAfterWait('layout_builder_configure_section');
     $page->fillField('layout_settings[setting_1]', 'Test Validation Error Message');
     $page->pressButton('Add section');
@@ -481,7 +487,8 @@ class LayoutBuilderTest extends WebDriverTestBase {
    */
   private function assertOffCanvasFormAfterWait(string $expected_form_id): void {
     $this->assertSession()->assertWaitOnAjaxRequest();
-    $off_canvas = $this->assertSession()->waitForElementVisible('css', '#drupal-off-canvas');
+    $this->waitForOffCanvasArea();
+    $off_canvas = $this->assertSession()->elementExists('css', '#drupal-off-canvas');
     $this->assertNotNull($off_canvas);
     $form_id_element = $off_canvas->find('hidden_field_selector', ['hidden_field', 'form_id']);
     // Ensure the form ID has the correct value and that the form is visible.
diff --git a/core/modules/system/tests/src/Traits/OffCanvasTestTrait.php b/core/modules/system/tests/src/Traits/OffCanvasTestTrait.php
index 80e226dee22..a406c6f44ae 100644
--- a/core/modules/system/tests/src/Traits/OffCanvasTestTrait.php
+++ b/core/modules/system/tests/src/Traits/OffCanvasTestTrait.php
@@ -18,6 +18,11 @@ trait OffCanvasTestTrait {
     // The data-resize-done attribute is added by the off_canvas_test module's
     // wrapper around Drupal.offCanvas.resetSize.
     $this->assertNotEmpty($this->assertSession()->waitForElementVisible('css', '[data-resize-done="true"]'));
+
+    // Remove the data-resize-done attribute so in scenarios where off-canvas
+    // opens yet another off-canvas, waitForOffCanvasArea() is looking for the
+    // attribute on a new dialog, not an existing one.
+    $this->getSession()->executeScript('document.querySelector("[data-resize-done]").removeAttribute("data-resize-done")');
   }
 
 }