diff --git a/core/modules/navigation/layouts/navigation.html.twig b/core/modules/navigation/layouts/navigation.html.twig
index 3748c239ea7..accf9e96f6d 100644
--- a/core/modules/navigation/layouts/navigation.html.twig
+++ b/core/modules/navigation/layouts/navigation.html.twig
@@ -70,6 +70,7 @@
         } only %}
       </div>
 
+      {{ content.content_top }}
       {{ content.content }}
     </nav>
 
diff --git a/core/modules/navigation/navigation.api.php b/core/modules/navigation/navigation.api.php
new file mode 100644
index 00000000000..f2824f29726
--- /dev/null
+++ b/core/modules/navigation/navigation.api.php
@@ -0,0 +1,57 @@
+<?php
+
+/**
+ * @file
+ * Hooks related to the Navigation module.
+ */
+
+/**
+ * @addtogroup hooks
+ * @{
+ */
+
+/**
+ * Provide content for Navigation content_top section.
+ *
+ * @return array
+ *   An associative array of renderable elements.
+ *
+ * @see hook_navigation_content_top_alter()
+ */
+function hook_navigation_content_top(): array {
+  return [
+    'navigation_foo' => [
+      '#markup' => \Drupal::config('system.site')->get('name'),
+      '#cache' => [
+        'tags' => ['config:system.site'],
+      ],
+    ],
+    'navigation_bar' => [
+      '#markup' => 'bar',
+    ],
+    'navigation_baz' => [
+      '#markup' => 'baz',
+    ],
+  ];
+}
+
+/**
+ * Alter replacement values for placeholder tokens.
+ *
+ * @param $content_top
+ *   An associative array of content returned by hook_navigation_content_top().
+ *
+ * @see hook_navigation_content_top()
+ */
+function hook_navigation_content_top_alter(array &$content_top): void {
+  // Remove a specific element.
+  unset($content_top['navigation_foo']);
+  // Modify an element.
+  $content_top['navigation_bar']['#markup'] = 'new bar';
+  // Change weight.
+  $content_top['navigation_baz']['#weight'] = '-100';
+}
+
+/**
+ * @} End of "addtogroup hooks".
+ */
diff --git a/core/modules/navigation/src/Hook/NavigationHooks.php b/core/modules/navigation/src/Hook/NavigationHooks.php
index 17d9b618d93..eb1ddb5b3a2 100644
--- a/core/modules/navigation/src/Hook/NavigationHooks.php
+++ b/core/modules/navigation/src/Hook/NavigationHooks.php
@@ -99,6 +99,11 @@ class NavigationHooks {
       ],
     ];
     $items['menu_region__footer'] = ['variables' => ['items' => [], 'title' => NULL, 'menu_name' => NULL]];
+    $items['navigation_content_top'] = [
+      'variables' => [
+        'items' => [],
+      ],
+    ];
     return $items;
   }
 
diff --git a/core/modules/navigation/src/NavigationRenderer.php b/core/modules/navigation/src/NavigationRenderer.php
index cb3ecaa0ea1..8e29298092d 100644
--- a/core/modules/navigation/src/NavigationRenderer.php
+++ b/core/modules/navigation/src/NavigationRenderer.php
@@ -3,6 +3,7 @@
 namespace Drupal\navigation;
 
 use Drupal\Component\Utility\NestedArray;
+use Drupal\Component\Utility\SortArray;
 use Drupal\Core\Block\BlockPluginInterface;
 use Drupal\Core\Cache\CacheBackendInterface;
 use Drupal\Core\Cache\CacheableMetadata;
@@ -18,6 +19,7 @@ use Drupal\Core\Image\ImageFactory;
 use Drupal\Core\Menu\LocalTaskManagerInterface;
 use Drupal\Core\Plugin\Context\Context;
 use Drupal\Core\Plugin\Context\ContextDefinition;
+use Drupal\Core\Render\Element;
 use Drupal\Core\Routing\RouteMatchInterface;
 use Drupal\Core\Security\Attribute\TrustedCallback;
 use Drupal\Core\Session\AccountInterface;
@@ -128,6 +130,7 @@ final class NavigationRenderer {
     if ($storage) {
       foreach ($storage->getSections() as $delta => $section) {
         $build[$delta] = $section->toRenderArray([]);
+        $build[$delta]['#cache']['contexts'] = ['user.permissions', 'theme', 'languages:language_interface'];
       }
     }
     // The render array is built based on decisions made by SectionStorage
@@ -157,6 +160,8 @@ final class NavigationRenderer {
     ];
     $build[0] = NestedArray::mergeDeepArray([$build[0], $defaults]);
 
+    $build[0]['content_top'] = $this->getContentTop();
+
     if ($logo_provider === self::LOGO_PROVIDER_CUSTOM) {
       $logo_path = $logo_settings->get('logo.path');
       if (!empty($logo_path) && is_file($logo_path)) {
@@ -169,10 +174,36 @@ final class NavigationRenderer {
         }
       }
     }
-    $build[0]['#cache']['contexts'] = ['user.permissions', 'theme', 'languages:language_interface'];
     return $build;
   }
 
+  /**
+   * Gets the content for content_top section.
+   *
+   * @return array
+   *   The content_top section content.
+   */
+  protected function getContentTop(): array {
+    $content_top = [
+      '#theme' => 'navigation_content_top',
+    ];
+    $content_top_items = $this->moduleHandler->invokeAll('navigation_content_top');
+    $this->moduleHandler->alter('navigation_content_top', $content_top_items);
+    uasort($content_top_items, [SortArray::class, 'sortByWeightElement']);
+    // Filter out empty items, taking care to merge any cacheability metadata.
+    $cacheability = new CacheableMetadata();
+    $content_top_items = array_filter($content_top_items, function ($item) use (&$cacheability) {
+      if (Element::isEmpty($item)) {
+        $cacheability = $cacheability->merge(CacheableMetadata::createFromRenderArray($item));
+        return FALSE;
+      }
+      return TRUE;
+    });
+    $cacheability->applyTo($content_top);
+    $content_top['#items'] = $content_top_items;
+    return $content_top;
+  }
+
   /**
    * Build the top bar for content entity pages.
    *
diff --git a/core/modules/navigation/templates/navigation-content-top.html.twig b/core/modules/navigation/templates/navigation-content-top.html.twig
new file mode 100644
index 00000000000..ba9c002d4cf
--- /dev/null
+++ b/core/modules/navigation/templates/navigation-content-top.html.twig
@@ -0,0 +1,17 @@
+{#
+/**
+ * @file
+ * Default theme implementation to display the navigation content_top section.
+ *
+ * Available variables:
+ * - items: An associative array of renderable elements to display in the
+ *   content_top section.
+ *
+ * @ingroup themeable
+ */
+#}
+{% if items is not empty %}
+  <div class="admin-toolbar__content-top">
+    {{ items }}
+  </div>
+{% endif %}
diff --git a/core/modules/navigation/tests/navigation_test/src/Hook/NavigationTestHooks.php b/core/modules/navigation/tests/navigation_test/src/Hook/NavigationTestHooks.php
index 2333d04f603..7071cee422c 100644
--- a/core/modules/navigation/tests/navigation_test/src/Hook/NavigationTestHooks.php
+++ b/core/modules/navigation/tests/navigation_test/src/Hook/NavigationTestHooks.php
@@ -4,6 +4,7 @@ declare(strict_types=1);
 
 namespace Drupal\navigation_test\Hook;
 
+use Drupal\Core\Cache\CacheableMetadata;
 use Drupal\Core\Hook\Attribute\Hook;
 use Drupal\Core\State\StateInterface;
 
@@ -34,4 +35,53 @@ class NavigationTestHooks {
     }
   }
 
+  /**
+   * Implements hook_navigation_content_top().
+   */
+  #[Hook('navigation_content_top')]
+  public function navigationContentTop(): array {
+    if (\Drupal::keyValue('navigation_test')->get('content_top')) {
+      $items = [
+        'navigation_foo' => [
+          '#markup' => 'foo',
+        ],
+        'navigation_bar' => [
+          '#markup' => 'bar',
+        ],
+        'navigation_baz' => [
+          '#markup' => 'baz',
+        ],
+      ];
+    }
+    else {
+      $items = [
+        'navigation_foo' => [],
+        'navigation_bar' => [],
+        'navigation_baz' => [],
+      ];
+    }
+    // Add cache tags to our items to express a made up dependency to test
+    // cacheability. Note that as we're always returning the same items,
+    // sometimes only with cacheability metadata. By doing this we're testing
+    // conditional rendering of content_top items.
+    foreach ($items as &$element) {
+      CacheableMetadata::createFromRenderArray($element)
+        ->addCacheTags(['navigation_test'])
+        ->applyTo($element);
+    }
+    return $items;
+  }
+
+  /**
+   * Implements hook_navigation_content_top_alter().
+   */
+  #[Hook('navigation_content_top_alter')]
+  public function navigationContentTopAlter(&$content_top): void {
+    if (\Drupal::keyValue('navigation_test')->get('content_top_alter')) {
+      unset($content_top['navigation_foo']);
+      $content_top['navigation_bar']['#markup'] = 'new bar';
+      $content_top['navigation_baz']['#weight'] = '-100';
+    }
+  }
+
 }
diff --git a/core/modules/navigation/tests/src/Functional/NavigationContentTopTest.php b/core/modules/navigation/tests/src/Functional/NavigationContentTopTest.php
new file mode 100644
index 00000000000..981b628259c
--- /dev/null
+++ b/core/modules/navigation/tests/src/Functional/NavigationContentTopTest.php
@@ -0,0 +1,58 @@
+<?php
+
+declare(strict_types=1);
+
+namespace Drupal\Tests\navigation\Functional;
+
+use Drupal\Core\Cache\Cache;
+use Drupal\Core\Url;
+use Drupal\Tests\BrowserTestBase;
+
+// cspell:ignore foobarbaz baznew
+
+/**
+ * Tests for navigation content_top section.
+ *
+ * @group navigation
+ */
+class NavigationContentTopTest extends BrowserTestBase {
+
+  /**
+   * {@inheritdoc}
+   */
+  protected static $modules = ['navigation', 'navigation_test', 'test_page_test'];
+
+  /**
+   * {@inheritdoc}
+   */
+  protected $defaultTheme = 'stark';
+
+  /**
+   * {@inheritdoc}
+   */
+  protected function setUp(): void {
+    parent::setUp();
+
+    $this->drupalLogin($this->createUser([
+      'access navigation',
+    ]));
+  }
+
+  /**
+   * Tests behavior of content_top section hooks.
+   */
+  public function testNavigationContentTop(): void {
+    $test_page_url = Url::fromRoute('test_page_test.test_page');
+    $this->drupalGet($test_page_url);
+    $this->assertSession()->elementNotExists('css', '.admin-toolbar__content-top');
+    \Drupal::keyValue('navigation_test')->set('content_top', 1);
+    Cache::invalidateTags(['navigation_test']);
+    $this->drupalGet($test_page_url);
+    $this->assertSession()->elementTextContains('css', '.admin-toolbar__content-top', 'foobarbaz');
+    \Drupal::keyValue('navigation_test')->set('content_top_alter', 1);
+    Cache::invalidateTags(['navigation_test']);
+    $this->drupalGet($test_page_url);
+    $this->assertSession()->elementTextContains('css', '.admin-toolbar__content-top', 'baznew bar');
+  }
+
+}