diff --git a/core/modules/outside_in/src/Block/BlockEntityOffCanvasForm.php b/core/modules/outside_in/src/Block/BlockEntityOffCanvasForm.php
index 19a701638d..8e74754fdb 100644
--- a/core/modules/outside_in/src/Block/BlockEntityOffCanvasForm.php
+++ b/core/modules/outside_in/src/Block/BlockEntityOffCanvasForm.php
@@ -5,8 +5,10 @@
 use Drupal\block\BlockForm;
 use Drupal\block\BlockInterface;
 use Drupal\Core\Block\BlockPluginInterface;
+use Drupal\Core\Form\DialogFormTrait;
 use Drupal\Core\Form\FormStateInterface;
 use Drupal\Core\Plugin\PluginWithFormsInterface;
+use Drupal\outside_in\OffCanvasFormDialogTrait;
 
 /**
  * Provides form for block instance forms when used in the off-canvas dialog.
@@ -18,6 +20,8 @@
  */
 class BlockEntityOffCanvasForm extends BlockForm {
 
+  use OffCanvasFormDialogTrait;
+
   /**
    * Provides a title callback to get the block's admin label.
    *
@@ -111,4 +115,24 @@ protected function getPluginForm(BlockPluginInterface $block) {
     return $block;
   }
 
+  /**
+   * {@inheritdoc}
+   */
+  public function submitForm(array &$form, FormStateInterface $form_state) {
+    parent::submitForm($form, $form_state);
+    // \Drupal\block\BlockForm::submitForm() always redirects to block listing
+    // via \Drupal\Core\Form\FormStateInterface::setRedirect(). This method
+    // does not work with Ajax submit.
+    $form_state->disableRedirect();
+  }
+
+  /**
+   * {@inheritdoc}
+   */
+  public function buildForm(array $form, FormStateInterface $form_state) {
+    $form = parent::buildForm($form, $form_state);
+    $this->buildFormDialog($form, $form_state, FALSE, '#drupal-off-canvas');
+    return $form;
+  }
+
 }
diff --git a/core/modules/outside_in/src/OffCanvasFormDialogTrait.php b/core/modules/outside_in/src/OffCanvasFormDialogTrait.php
new file mode 100644
index 0000000000..990d897e4f
--- /dev/null
+++ b/core/modules/outside_in/src/OffCanvasFormDialogTrait.php
@@ -0,0 +1,160 @@
+<?php
+
+namespace Drupal\outside_in;
+
+use Drupal\Core\Ajax\AjaxResponse;
+use Drupal\Core\Ajax\RedirectCommand;
+use Drupal\Core\Ajax\ReplaceCommand;
+use Drupal\Core\EventSubscriber\MainContentViewSubscriber;
+use Drupal\Core\Form\FormStateInterface;
+use Drupal\Core\Url;
+
+/**
+ * Helper trait for forms that are used in the off-canvas dialog.
+ *
+ * Classes that use this trait should implement \Drupal\Core\Form\FormInterface.
+ *
+ * @internal
+ *   This trait will likely be replace with a common API for handling form
+ *   submissions in dialogs.
+ *   @todo Remove in https://www.drupal.org/node/2896535.
+ */
+trait OffCanvasFormDialogTrait {
+
+  /**
+   * Determines if the current request is for an AJAX modal dialog.
+   *
+   * @return bool
+   *   TRUE is the current request if for an AJAX modal dialog.
+   */
+  protected function isOffCanvasDialog() {
+    $wrapper_format = $this->getRequest()
+      ->get(MainContentViewSubscriber::WRAPPER_FORMAT);
+    return $wrapper_format === 'drupal_dialog.off_canvas';
+  }
+
+  /**
+   * Adds modal dialog support to a form.
+   *
+   * @param array $form
+   *   An associative array containing the structure of the form.
+   * @param \Drupal\Core\Form\FormStateInterface $form_state
+   *   The current state of the form.
+   */
+  protected function buildFormDialog(array &$form, FormStateInterface $form_state) {
+    if (!$this->isOffCanvasDialog()) {
+      return;
+    }
+
+    $form['actions']['submit']['#ajax'] = [
+      'dialogType' => $this->getDialogType(),
+      'dialogRenderer' => $this->getDialogRenderer(),
+      'callback' => '::submitFormDialog',
+      'event' => 'click',
+    ];
+
+    $form['#attached']['library'][] = 'core/drupal.dialog.ajax';
+    $form['#attributes']['id'] = 'off-canvas-form';
+  }
+
+  /**
+   * @return mixed
+   */
+  protected function getRequestWrapperFormat() {
+    $wrapper_format = $this->getRequest()
+      ->get(MainContentViewSubscriber::WRAPPER_FORMAT);
+    return $wrapper_format;
+  }
+  /**
+   *
+   */
+  protected function getDialogType() {
+    $wrapper_format = $this->getRequestWrapperFormat();
+    $wrapper_format_parts = explode('.', $wrapper_format);
+    // Remove the "drupal_" prefix.
+    return substr($wrapper_format_parts[0], 7);
+  }
+
+  /**
+   *
+   */
+  protected function getDialogRenderer() {
+    $wrapper_format = $this->getRequestWrapperFormat();
+    $wrapper_format_parts = explode('.', $wrapper_format);
+    return isset($wrapper_format_parts[1]) ? $wrapper_format_parts[1] : NULL;
+  }
+
+  /**
+   * Submit form dialog #ajax callback.
+   *
+   * @param array $form
+   *   An associative array containing the structure of the form.
+   * @param \Drupal\Core\Form\FormStateInterface $form_state
+   *   The current state of the form.
+   *
+   * @return \Drupal\Core\Ajax\AjaxResponse
+   *   An AJAX response that display validation error messages or redirects
+   *   to a URL
+   */
+  public function submitFormDialog(array &$form, FormStateInterface $form_state) {
+    $response = new AjaxResponse();
+    if ($form_state->hasAnyErrors()) {
+      $form['status_messages'] = [
+        '#type' => 'status_messages',
+        '#weight' => -1000,
+      ];
+      $command = new ReplaceCommand('#off-canvas-form', $form);
+    }
+    else {
+      if ($redirect_url = $this->getRedirectUrl()) {
+        $command = new RedirectCommand($redirect_url->setAbsolute()->toString());
+      }
+      else {
+        // Settings Tray always provides a destination.
+        throw new \Exception("No destination provide for Settings Tray form");
+      }
+    }
+    return $response->addCommand($command);
+  }
+
+  /**
+   * Gets the form's redirect URL.
+   *
+   * Isolate a form's redirect URL/destination so that it can be used by
+   * ::submitFormDialog or ::submitForm.
+   *
+   * @return \Drupal\Core\Url|null
+   *   The redirect URL or NULL if dialog should just be closed.
+   */
+  protected function getRedirectUrl() {
+    return $this->getDestinationUrl();
+  }
+
+  /**
+   * Gets the URL from the destination service.
+   *
+   * @return \Drupal\Core\Url|null
+   *   The destination URL or NULL no destination available.
+   */
+  protected function getDestinationUrl() {
+    if ($destination = $this->getRedirectDestinationPath()) {
+      return Url::fromUserInput('/' . $destination);
+    }
+  }
+
+  /**
+   * Gets the redirect destination path if specified in request.
+   *
+   * \Drupal\Core\Routing\RedirectDestination::get() cannot be used directly
+   * because it will use <current> if 'destination' is not in the query string.
+   *
+   * @return string|null
+   *   The redirect path or NULL if it is not specified.
+   */
+  protected function getRedirectDestinationPath() {
+    if ($this->requestStack->getCurrentRequest()->get('destination')) {
+      return $this->getRedirectDestination()->get();
+    }
+  }
+
+}
diff --git a/core/modules/outside_in/tests/modules/off_canvas_test/off_canvas_test.routing.yml b/core/modules/outside_in/tests/modules/off_canvas_test/off_canvas_test.routing.yml
index 4ae56c4ee8..f0b3a43653 100644
--- a/core/modules/outside_in/tests/modules/off_canvas_test/off_canvas_test.routing.yml
+++ b/core/modules/outside_in/tests/modules/off_canvas_test/off_canvas_test.routing.yml
@@ -27,3 +27,10 @@ off_canvas_test.dialog_links:
     _controller: '\Drupal\off_canvas_test\Controller\TestController::otherDialogLinks'
   requirements:
     _access: 'TRUE'
+
+off_canvas_test.form:
+  path: '/off-canvas-form'
+  defaults:
+    _form: '\Drupal\off_canvas_test\Form\TestForm'
+  requirements:
+    _access: 'TRUE'
diff --git a/core/modules/outside_in/tests/modules/off_canvas_test/src/Controller/TestController.php b/core/modules/outside_in/tests/modules/off_canvas_test/src/Controller/TestController.php
index 6164b06fc2..58bebc3a0b 100644
--- a/core/modules/outside_in/tests/modules/off_canvas_test/src/Controller/TestController.php
+++ b/core/modules/outside_in/tests/modules/off_canvas_test/src/Controller/TestController.php
@@ -92,6 +92,25 @@ public function linksDisplay() {
           ],
         ],
       ],
+      'off_canvas_form' => [
+        '#title' => 'Show form!',
+        '#type' => 'link',
+        '#url' => Url::fromRoute(
+          'off_canvas_test.form',
+          [],
+          ['query' => ['destination' => 'off-canvas-test-links']]
+        ),
+        '#attributes' => [
+          'class' => ['use-ajax'],
+          'data-dialog-type' => 'dialog',
+          'data-dialog-renderer' => 'off_canvas',
+        ],
+        '#attached' => [
+          'library' => [
+            'outside_in/drupal.outside_in',
+          ],
+        ],
+      ],
     ];
   }
 
diff --git a/core/modules/outside_in/tests/modules/off_canvas_test/src/Form/TestForm.php b/core/modules/outside_in/tests/modules/off_canvas_test/src/Form/TestForm.php
new file mode 100644
index 0000000000..a9a4350042
--- /dev/null
+++ b/core/modules/outside_in/tests/modules/off_canvas_test/src/Form/TestForm.php
@@ -0,0 +1,59 @@
+<?php
+
+namespace Drupal\off_canvas_test\Form;
+
+use Drupal\Core\Form\FormBase;
+use Drupal\Core\Form\FormStateInterface;
+use Drupal\outside_in\OffCanvasFormDialogTrait;
+
+/**
+ * Just a test form.
+ */
+class TestForm extends FormBase {
+
+  use OffCanvasFormDialogTrait;
+
+  /**
+   * {@inheritdoc}
+   */
+  public function getFormId() {
+    return "off_canvas_test_form";
+  }
+
+  /**
+   * {@inheritdoc}
+   */
+  public function buildForm(array $form, FormStateInterface $form_state) {
+    $form['force_error'] = [
+      '#type' => 'checkbox',
+      '#title' => $this->t('Force error?'),
+    ];
+    $form['actions'] = [
+      '#type' => 'actions',
+      'submit' => [
+        '#type' => 'submit',
+        '#value' => $this->t('Submit'),
+      ],
+    ];
+    $this->buildFormDialog($form, $form_state);
+    return $form;
+  }
+
+  /**
+   * {@inheritdoc}
+   */
+  public function validateForm(array &$form, FormStateInterface $form_state) {
+    parent::validateForm($form, $form_state);
+    if ($form_state->getValue('force_error')) {
+      $form_state->setErrorByName('force_error', 'Validation error');
+    }
+  }
+
+  /**
+   * {@inheritdoc}
+   */
+  public function submitForm(array &$form, FormStateInterface $form_state) {
+    drupal_set_message('submitted');
+  }
+
+}
diff --git a/core/modules/outside_in/tests/src/FunctionalJavascript/OffCanvasTest.php b/core/modules/outside_in/tests/src/FunctionalJavascript/OffCanvasTest.php
index 2f64d9fe2c..a2bd7a46a5 100644
--- a/core/modules/outside_in/tests/src/FunctionalJavascript/OffCanvasTest.php
+++ b/core/modules/outside_in/tests/src/FunctionalJavascript/OffCanvasTest.php
@@ -120,4 +120,32 @@ protected function getTestThemes() {
     return array_merge(parent::getTestThemes(), ['seven']);
   }
 
+  /**
+   * Tests form errors in the Off-Canvas dialog.
+   */
+  public function testFormErrors() {
+    $web_assert = $this->assertSession();
+    $page = $this->getSession()->getPage();
+
+    // Submit form with no error and sending a destination.
+    $this->drupalGet('/off-canvas-test-links');
+    $page->clickLink('Show form!');
+    $this->waitForOffCanvasToOpen();
+    $page->pressButton('Submit');
+    $web_assert->assertWaitOnAjaxRequest();
+    // Make sure the changes are present.
+    $this->assertNotEmpty($web_assert->waitForElement('css', 'div.messages.messages--status:contains(submitted)'));
+    $web_assert->elementNotContains('css', 'body', 'Validation error');
+
+    // Submit form with an error and sending a destination.
+    $this->drupalGet('/off-canvas-test-links');
+    $page->clickLink('Show form!');
+    $this->waitForOffCanvasToOpen();
+    $page->checkField('Force error?');
+    $page->pressButton('Submit');
+    $web_assert->assertWaitOnAjaxRequest();
+    $web_assert->elementNotContains('css', 'body', 'submitted');
+    $web_assert->elementContains('css', '#drupal-off-canvas', 'Validation error');
+  }
+
 }
diff --git a/core/modules/outside_in/tests/src/FunctionalJavascript/OutsideInBlockFormTest.php b/core/modules/outside_in/tests/src/FunctionalJavascript/OutsideInBlockFormTest.php
index 04fc230f5e..5d873388b5 100644
--- a/core/modules/outside_in/tests/src/FunctionalJavascript/OutsideInBlockFormTest.php
+++ b/core/modules/outside_in/tests/src/FunctionalJavascript/OutsideInBlockFormTest.php
@@ -114,10 +114,9 @@ public function testBlocks($block_plugin, $new_page_text, $element_selector, $la
       if (isset($new_page_text)) {
         $page->pressButton($button_text);
         // Make sure the changes are present.
-        // @todo Use a wait method that will take into account the form submitting
-        //   and all JavaScript activity. https://www.drupal.org/node/2837676
-        //   The use \Behat\Mink\WebAssert::pageTextContains to check text.
-        $this->assertJsCondition('jQuery("' . $block_selector . ' ' . $label_selector . '").html() == "' . $new_page_text . '"');
+        $new_page_text_locator = "$block_selector $label_selector:contains($new_page_text)";
+        $this->assertElementVisibleAfterWait('css', $new_page_text_locator);
+        $web_assert->assertWaitOnAjaxRequest();
       }
 
       $this->openBlockForm($block_selector);
@@ -131,7 +130,7 @@ public function testBlocks($block_plugin, $new_page_text, $element_selector, $la
       // Open block form by clicking a element inside the block.
       // This confirms that default action for links and form elements is
       // suppressed.
-      $this->openBlockForm("$block_selector {$element_selector}");
+      $this->openBlockForm("$block_selector {$element_selector}", $block_selector);
       $web_assert->elementTextContains('css', '.contextual-toolbar-tab button', 'Editing');
       $web_assert->elementAttributeContains('css', '.dialog-off-canvas__main-canvas', 'class', 'js-outside-in-edit-mode');
       // Simulate press the Escape key.
@@ -154,7 +153,7 @@ public function providerTestBlocks() {
     $blocks = [
       'block-powered' => [
         'block_plugin' => 'system_powered_by_block',
-        'new_page_text' => 'Can you imagine anyone showing the label on this block?',
+        'new_page_text' => 'Can you imagine anyone showing the label on this block',
         'element_selector' => 'span a',
         'label_selector' => 'h2',
         'button_text' => 'Save Powered by Drupal',
@@ -162,7 +161,7 @@ public function providerTestBlocks() {
       ],
       'block-branding' => [
         'block_plugin' => 'system_branding_block',
-        'new_page_text' => 'The site that will live a very short life.',
+        'new_page_text' => 'The site that will live a very short life',
         'element_selector' => "a[rel='home']:last-child",
         'label_selector' => "a[rel='home']:last-child",
         'button_text' => 'Save Site branding',
@@ -225,8 +224,20 @@ protected function assertOffCanvasBlockFormIsValid() {
    *
    * @param string $block_selector
    *   A css selector selects the block or an element within it.
+   * @param string $contextual_link_container
+   *   The element that contains the contextual links. If none provide the
+   *   $block_selector will be used.
    */
-  protected function openBlockForm($block_selector) {
+  protected function openBlockForm($block_selector, $contextual_link_container = '') {
+    if (!$contextual_link_container) {
+      $contextual_link_container = $block_selector;
+    }
+    // Ensure that contextual link element is present because this is required
+    // to open the off-canvas dialog in edit mode.
+    $contextual_link = $this->assertSession()->waitForElement('css', "$contextual_link_container .contextual-links a");
+    $this->assertNotEmpty($contextual_link);
+    // Ensure that all other Ajax activity is completed.
+    $this->assertSession()->assertWaitOnAjaxRequest();
     $this->click($block_selector);
     $this->waitForOffCanvasToOpen();
     $this->assertOffCanvasBlockFormIsValid();