diff --git a/core/core.services.yml b/core/core.services.yml
index 0b093c4669..0305f891e2 100644
--- a/core/core.services.yml
+++ b/core/core.services.yml
@@ -886,6 +886,10 @@ services:
   argument_resolver.default:
     class: Symfony\Component\HttpKernel\Controller\ArgumentResolver\DefaultValueResolver
     public: false
+  http_middleware.ajax_page_state:
+    class: Drupal\Core\StackMiddleware\AjaxPageState
+    tags:
+      - { name: http_middleware, priority: 500 }
   http_middleware.negotiation:
     class: Drupal\Core\StackMiddleware\NegotiationMiddleware
     tags:
diff --git a/core/lib/Drupal/Core/Ajax/SettingsCommand.php b/core/lib/Drupal/Core/Ajax/SettingsCommand.php
index ca41720dcb..5dbcaa600c 100644
--- a/core/lib/Drupal/Core/Ajax/SettingsCommand.php
+++ b/core/lib/Drupal/Core/Ajax/SettingsCommand.php
@@ -2,6 +2,8 @@
 
 namespace Drupal\Core\Ajax;
 
+use Drupal\Component\Utility\UrlHelper;
+
 /**
  * AJAX command for adjusting Drupal's JavaScript settings.
  *
@@ -53,6 +55,15 @@ public function __construct(array $settings, $merge = FALSE) {
    * Implements Drupal\Core\Ajax\CommandInterface:render().
    */
   public function render() {
+    if (isset($this->settings['ajax_page_state'])) {
+      // Get the current ajax_page_state that was passed to this request.
+      $ajax_page_state = \Drupal::requestStack()->getCurrentRequest()->get('ajax_page_state');
+
+      foreach ($this->settings as $key => $setting) {
+        $ajax_page_state[$key] = $setting;
+      }
+      $this->settings['ajax_page_state'] = UrlHelper::compressQueryParameter(json_encode($ajax_page_state));
+    }
 
     return [
       'command' => 'settings',
diff --git a/core/lib/Drupal/Core/Asset/AssetResolver.php b/core/lib/Drupal/Core/Asset/AssetResolver.php
index 04a5186368..37b5b34125 100644
--- a/core/lib/Drupal/Core/Asset/AssetResolver.php
+++ b/core/lib/Drupal/Core/Asset/AssetResolver.php
@@ -4,6 +4,7 @@
 
 use Drupal\Component\Utility\Crypt;
 use Drupal\Component\Utility\NestedArray;
+use Drupal\Component\Utility\UrlHelper;
 use Drupal\Core\Cache\CacheBackendInterface;
 use Drupal\Core\Extension\ModuleHandlerInterface;
 use Drupal\Core\Language\LanguageManagerInterface;
@@ -335,6 +336,11 @@ public function getJsAssets(AttachedAssetsInterface $assets, $optimize, Language
       // Update the $assets object accordingly, so that it reflects the final
       // settings.
       $assets->setSettings($settings);
+      // Convert ajaxPageState to a compressed string from an array, since it is
+      // used by ajax.js to pass to AJAX requests as a query parameter.
+      if (isset($settings['ajaxPageState'])) {
+        $settings['ajaxPageState'] = UrlHelper::compressQueryParameter(json_encode($settings['ajaxPageState']));
+      }
       $settings_as_inline_javascript = [
         'type' => 'setting',
         'group' => JS_SETTING,
diff --git a/core/lib/Drupal/Core/StackMiddleware/AjaxPageState.php b/core/lib/Drupal/Core/StackMiddleware/AjaxPageState.php
new file mode 100644
index 0000000000..17ead34fa8
--- /dev/null
+++ b/core/lib/Drupal/Core/StackMiddleware/AjaxPageState.php
@@ -0,0 +1,42 @@
+<?php
+
+namespace Drupal\Core\StackMiddleware;
+
+use Drupal\Component\Utility\UrlHelper;
+use Symfony\Component\HttpFoundation\Request;
+use Symfony\Component\HttpFoundation\Response;
+use Symfony\Component\HttpKernel\HttpKernelInterface;
+
+/**
+ * Expands the compressed ajax_page_state query parameter into an array.
+ */
+class AjaxPageState implements HttpKernelInterface {
+
+  /**
+   * Constructs a new AjaxPageState instance.
+   *
+   * @param \Symfony\Component\HttpKernel\HttpKernelInterface $httpKernel
+   *   The wrapped HTTP kernel.
+   */
+  public function __construct(protected readonly HttpKernelInterface $httpKernel) {
+  }
+
+  /**
+   * {@inheritdoc}
+   */
+  public function handle(Request $request, $type = self::MAIN_REQUEST, $catch = TRUE): Response {
+    if ($request->request->has('ajax_page_state')) {
+      $ajax_page_state = $request->request->get('ajax_page_state');
+      $ajax_page_state = json_decode(UrlHelper::uncompressQueryParameter($ajax_page_state), TRUE);
+      $request->request->set('ajax_page_state', $ajax_page_state);
+    }
+    if ($request->query->has('ajax_page_state')) {
+      $ajax_page_state = $request->query->get('ajax_page_state');
+      $ajax_page_state = json_decode(UrlHelper::uncompressQueryParameter($ajax_page_state), TRUE);
+      $request->query->set('ajax_page_state', $ajax_page_state);
+      $request->request->set('ajax_page_state', $ajax_page_state);
+    }
+    return $this->httpKernel->handle($request, $type, $catch);
+  }
+
+}
diff --git a/core/lib/Drupal/Core/Theme/AjaxBasePageNegotiator.php b/core/lib/Drupal/Core/Theme/AjaxBasePageNegotiator.php
index ff50dc3eb0..80025daa6a 100644
--- a/core/lib/Drupal/Core/Theme/AjaxBasePageNegotiator.php
+++ b/core/lib/Drupal/Core/Theme/AjaxBasePageNegotiator.php
@@ -66,7 +66,7 @@ public function __construct(CsrfTokenGenerator $token_generator, ConfigFactoryIn
    */
   public function applies(RouteMatchInterface $route_match) {
     $ajax_page_state = $this->requestStack->getCurrentRequest()->get('ajax_page_state');
-    return !empty($ajax_page_state['theme']) && isset($ajax_page_state['theme_token']);
+    return !empty($ajax_page_state['theme']);
   }
 
   /**
diff --git a/core/misc/ajax.js b/core/misc/ajax.js
index 307fd81163..a601cba41d 100644
--- a/core/misc/ajax.js
+++ b/core/misc/ajax.js
@@ -824,13 +824,11 @@
 
     // Allow Drupal to return new JavaScript and CSS files to load without
     // returning the ones already loaded.
+    // @see \Drupal\Core\StackMiddleWare\AjaxPageState
     // @see \Drupal\Core\Theme\AjaxBasePageNegotiator
     // @see \Drupal\Core\Asset\LibraryDependencyResolverInterface::getMinimalRepresentativeSubset()
     // @see system_js_settings_alter()
-    const pageState = drupalSettings.ajaxPageState;
-    options.data['ajax_page_state[theme]'] = pageState.theme;
-    options.data['ajax_page_state[theme_token]'] = pageState.theme_token;
-    options.data['ajax_page_state[libraries]'] = pageState.libraries;
+    options.data.ajax_page_state = drupalSettings.ajaxPageState;
   };
 
   /**
diff --git a/core/modules/system/tests/src/Functional/Render/AjaxPageStateTest.php b/core/modules/system/tests/src/Functional/Render/AjaxPageStateTest.php
index 005769d38f..9dbf04b6d1 100644
--- a/core/modules/system/tests/src/Functional/Render/AjaxPageStateTest.php
+++ b/core/modules/system/tests/src/Functional/Render/AjaxPageStateTest.php
@@ -2,6 +2,7 @@
 
 namespace Drupal\Tests\system\Functional\Render;
 
+use Drupal\Component\Utility\UrlHelper;
 use Drupal\Tests\BrowserTestBase;
 
 /**
@@ -69,9 +70,7 @@ public function testDrupalSettingsIsNotLoaded() {
       [
         "query" =>
           [
-            'ajax_page_state' => [
-              'libraries' => 'core/drupalSettings',
-            ],
+            'ajax_page_state' => UrlHelper::compressQueryParameter(json_encode(['libraries' => 'core/drupalSettings'])),
           ],
       ]
     );
@@ -90,7 +89,7 @@ public function testDrupalSettingsIsNotLoaded() {
    */
   public function testMultipleLibrariesAreNotLoaded() {
     $this->drupalGet('node',
-      ['query' => ['ajax_page_state' => ['libraries' => 'core/drupal,core/drupalSettings']]]
+      ['query' => ['ajax_page_state' => UrlHelper::compressQueryParameter(json_encode(['libraries' => 'core/drupal,core/drupalSettings']))]]
     );
     $this->assertSession()->statusCodeEquals(200);
     // The drupal library from core should be excluded from loading.
diff --git a/core/tests/Drupal/FunctionalJavascriptTests/Ajax/AjaxTest.php b/core/tests/Drupal/FunctionalJavascriptTests/Ajax/AjaxTest.php
index be8dae2657..49de1f4c37 100644
--- a/core/tests/Drupal/FunctionalJavascriptTests/Ajax/AjaxTest.php
+++ b/core/tests/Drupal/FunctionalJavascriptTests/Ajax/AjaxTest.php
@@ -2,6 +2,7 @@
 
 namespace Drupal\FunctionalJavascriptTests\Ajax;
 
+use Drupal\Component\Utility\UrlHelper;
 use Drupal\FunctionalJavascriptTests\WebDriverTestBase;
 
 /**
@@ -37,7 +38,7 @@ public function testAjaxWithAdminRoute() {
     $assert = $this->assertSession();
     $assert->pageTextContains('Current theme: claro');
 
-    // Now click the modal, which should also use the admin theme.
+    // Now click the modal, which should use the front-end theme.
     $this->drupalGet('ajax-test/dialog');
     $assert->pageTextNotContains('Current theme: stable9');
     $this->clickLink('Link 8 (ajax)');
@@ -59,32 +60,40 @@ public function testDrupalSettingsCachingRegression() {
 
     // Insert a fake library into the already loaded library settings.
     $fake_library = 'fakeLibrary/fakeLibrary';
-    $session->evaluateScript("drupalSettings.ajaxPageState.libraries = drupalSettings.ajaxPageState.libraries + ',$fake_library';");
-
-    $libraries = $session->evaluateScript('drupalSettings.ajaxPageState.libraries');
+    $ajax_page_state = $session->evaluateScript("drupalSettings.ajaxPageState");
+    $ajax_page_state = json_decode(UrlHelper::uncompressQueryParameter($ajax_page_state), 1);
+    $ajax_page_state['libraries'] = $ajax_page_state['libraries'] . $fake_library;
+    $ajax_page_state = UrlHelper::compressQueryParameter(json_encode($ajax_page_state));
+    $session->evaluateScript("drupalSettings.ajaxPageState = '$ajax_page_state';");
+    $ajax_page_state = $session->evaluateScript("drupalSettings.ajaxPageState");
+    $ajax_page_state = json_decode(UrlHelper::uncompressQueryParameter($ajax_page_state), 1);
     // Test that the fake library is set.
-    $this->assertStringContainsString($fake_library, $libraries);
+    $this->assertStringContainsString($fake_library, $ajax_page_state['libraries']);
 
     // Click on the AJAX link.
     $this->clickLink('Link 8 (ajax)');
     $assert->assertWaitOnAjaxRequest();
 
     // Test that the fake library is still set after the AJAX call.
-    $libraries = $session->evaluateScript('drupalSettings.ajaxPageState.libraries');
-    $this->assertStringContainsString($fake_library, $libraries);
+    $ajax_page_state = $session->evaluateScript("drupalSettings.ajaxPageState");
+    $ajax_page_state = json_decode(UrlHelper::uncompressQueryParameter($ajax_page_state), 1);
+    // Test that the fake library is set.
+    $this->assertStringContainsString($fake_library, $ajax_page_state['libraries']);
 
     // Reload the page, this should reset the loaded libraries and remove the
     // fake library.
     $this->drupalGet('ajax-test/dialog');
-    $libraries = $session->evaluateScript('drupalSettings.ajaxPageState.libraries');
-    $this->assertStringNotContainsString($fake_library, $libraries);
+    $ajax_page_state = $session->evaluateScript("drupalSettings.ajaxPageState");
+    $ajax_page_state = json_decode(UrlHelper::uncompressQueryParameter($ajax_page_state), 1);
+    $this->assertStringNotContainsString($fake_library, $ajax_page_state['libraries']);
 
     // Click on the AJAX link again, and the libraries should still not contain
     // the fake library.
     $this->clickLink('Link 8 (ajax)');
     $assert->assertWaitOnAjaxRequest();
-    $libraries = $session->evaluateScript('drupalSettings.ajaxPageState.libraries');
-    $this->assertStringNotContainsString($fake_library, $libraries);
+    $ajax_page_state = $session->evaluateScript("drupalSettings.ajaxPageState");
+    $ajax_page_state = json_decode(UrlHelper::uncompressQueryParameter($ajax_page_state), 1);
+    $this->assertStringNotContainsString($fake_library, $ajax_page_state['libraries']);
   }
 
   /**
diff --git a/core/tests/Drupal/FunctionalJavascriptTests/WebDriverTestBase.php b/core/tests/Drupal/FunctionalJavascriptTests/WebDriverTestBase.php
index e3f011c554..91d69bc544 100644
--- a/core/tests/Drupal/FunctionalJavascriptTests/WebDriverTestBase.php
+++ b/core/tests/Drupal/FunctionalJavascriptTests/WebDriverTestBase.php
@@ -3,6 +3,7 @@
 namespace Drupal\FunctionalJavascriptTests;
 
 use Behat\Mink\Exception\DriverException;
+use Drupal\Component\Utility\UrlHelper;
 use Drupal\Tests\BrowserTestBase;
 use PHPUnit\Runner\BaseTestRunner;
 use Symfony\Component\DependencyInjection\ContainerInterface;
@@ -204,12 +205,15 @@ public function assertSession($name = NULL) {
    * current values of drupalSettings, capturing all changes made via javascript
    * after the page was loaded.
    *
+   * @param bool $uncompress_ajax_page_state
+   *   Whether to uncompress ajax_page_state, defaults to TRUE.
+   *
    * @return array
    *   The Drupal javascript settings array.
    *
    * @see \Drupal\Tests\BrowserTestBase::getDrupalSettings()
    */
-  protected function getDrupalSettings() {
+  protected function getDrupalSettings(bool $uncompress_ajax_page_state = TRUE) {
     $script = <<<EndOfScript
 (function () {
   if (typeof drupalSettings !== 'undefined') {
@@ -217,8 +221,11 @@ protected function getDrupalSettings() {
   }
 })();
 EndOfScript;
-
-    return $this->getSession()->evaluateScript($script) ?: [];
+    $settings = $this->getSession()->evaluateScript($script) ?: [];
+    if (isset($settings['ajaxPageState']) && $uncompress_ajax_page_state) {
+      $settings['ajaxPageState'] = json_decode(UrlHelper::uncompressQueryParameter($settings['ajaxPageState']), 1);
+    }
+    return $settings;
   }
 
   /**
diff --git a/core/tests/Drupal/Tests/BrowserTestBase.php b/core/tests/Drupal/Tests/BrowserTestBase.php
index 3d3e41c51d..86bf74010f 100644
--- a/core/tests/Drupal/Tests/BrowserTestBase.php
+++ b/core/tests/Drupal/Tests/BrowserTestBase.php
@@ -8,6 +8,7 @@
 use Behat\Mink\Selector\SelectorsHandler;
 use Behat\Mink\Session;
 use Drupal\Component\Serialization\Json;
+use Drupal\Component\Utility\UrlHelper;
 use Drupal\Core\Database\Database;
 use Drupal\Core\Test\FunctionalTestSetupTrait;
 use Drupal\Core\Test\TestSetupTrait;
@@ -626,13 +627,20 @@ protected function config($name) {
   /**
    * Gets the JavaScript drupalSettings variable for the currently-loaded page.
    *
+   * @param bool $uncompress_ajax_page_state
+   *   Whether to uncompress ajax_page_state, defaults to TRUE.
+   *
    * @return array
    *   The JSON decoded drupalSettings value from the current page.
    */
-  protected function getDrupalSettings() {
+  protected function getDrupalSettings(bool $uncompress_ajax_page_state = TRUE) {
     $html = $this->getSession()->getPage()->getContent();
     if (preg_match('@<script type="application/json" data-drupal-selector="drupal-settings-json">([^<]*)</script>@', $html, $matches)) {
-      return Json::decode($matches[1]);
+      $settings = Json::decode($matches[1]);
+      if (isset($settings['ajaxPageState']) && $uncompress_ajax_page_state) {
+        $settings['ajaxPageState'] = json_decode(UrlHelper::uncompressQueryParameter($settings['ajaxPageState']), 1);
+      }
+      return $settings;
     }
     return [];
   }