diff --git a/ext/afform/mock/ang/testMultipleSearchForm.aff.html b/ext/afform/mock/ang/testMultipleSearchForm.aff.html
new file mode 100644
index 000000000000..3d60563fafa1
--- /dev/null
+++ b/ext/afform/mock/ang/testMultipleSearchForm.aff.html
@@ -0,0 +1,21 @@
+<div>
+  <div af-fieldset="">
+    <af-field name="source" />
+    <af-field name="Contact_Email_contact_id_01.location_type_id" defn="{input_attrs: {multiple: true}}" />
+    <crm-search-display-table search-name="TestContactEmailSearch" display-name="TestContactEmailDisplay"></crm-search-display-table>
+  </div>
+  <div af-fieldset="">
+    <!-- Filter is in wrong fieldset to work with `TestSearchForEmail`. See SearchAfformTest::testRunMultipleSearchForm -->
+    <af-field name="email" />
+    <crm-search-display-table search-name="TestContactEmailSearch" display-name=""></crm-search-display-table>
+  </div>
+</div>
+<div af-fieldset="">
+  <af-field name="contact_id.display_name" />
+  <af-field name="location_type_id" />
+  <crm-search-display-table search-name="TestSearchForEmail" display-name=""></crm-search-display-table>
+</div>
+<!-- This display is not enclosed in an af-fieldset so this filter will not work. See SearchAfformTest::testRunMultipleSearchForm -->
+<af-field name="location_type_id" />
+<crm-search-display-table filters="{'contact_id.display_name': 'testRunMultipleSearchForm'}" search-name="TestSearchForPhone" display-name=""></crm-search-display-table>
+
diff --git a/ext/afform/mock/ang/testMultipleSearchForm.aff.json b/ext/afform/mock/ang/testMultipleSearchForm.aff.json
new file mode 100644
index 000000000000..609e0f5033cf
--- /dev/null
+++ b/ext/afform/mock/ang/testMultipleSearchForm.aff.json
@@ -0,0 +1,6 @@
+{
+    "type": "search",
+    "title": "TestMultipleSearchForm",
+    "server_route": "",
+    "permission": "access CiviCRM"
+}
diff --git a/ext/search_kit/Civi/Api4/Action/SearchDisplay/AbstractRunAction.php b/ext/search_kit/Civi/Api4/Action/SearchDisplay/AbstractRunAction.php
index abf81cd7d53c..6d63a56d8ff1 100644
--- a/ext/search_kit/Civi/Api4/Action/SearchDisplay/AbstractRunAction.php
+++ b/ext/search_kit/Civi/Api4/Action/SearchDisplay/AbstractRunAction.php
@@ -999,7 +999,7 @@ private function getAfformFilters() {
     }
     // Get afform field filters
     $filterKeys = array_column(\CRM_Utils_Array::findAll(
-      $afform['layout'] ?? [],
+      $afform['searchDisplay']['fieldset'],
       ['#tag' => 'af-field']
     ), 'name');
     // Get filters passed into search display directive from Afform markup
@@ -1028,24 +1028,35 @@ private function getAfformFilters() {
    *
    * Verifies the searchDisplay is embedded in the afform and the user has permission to view it.
    *
-   * @return array|false|null
+   * @return array|false
    */
   private function loadAfform() {
     // Only attempt to load afform once.
     if ($this->afform && !isset($this->_afform)) {
       $this->_afform = FALSE;
       // Permission checks are enabled in this api call to ensure the user has permission to view the form
-      $afform = \Civi\Api4\Afform::get()
+      $afform = \Civi\Api4\Afform::get($this->getCheckPermissions())
         ->addWhere('name', '=', $this->afform)
-        ->setLayoutFormat('shallow')
+        ->setLayoutFormat('deep')
         ->execute()->first();
+      if (empty($afform['layout'])) {
+        return FALSE;
+      }
+      // Get all search display fieldsets (which will have an empty value for the af-fieldset attribute)
+      $fieldsets = \CRM_Utils_Array::findAll($afform['layout'], ['af-fieldset' => '']);
+      // As a fallback, search the entire afform in case the search display is not in a fieldset
+      $fieldsets['form'] = $afform['layout'];
       // Validate that the afform contains this search display
-      $afform['searchDisplay'] = \CRM_Utils_Array::findAll(
-          $afform['layout'] ?? [],
-          ['#tag' => "{$this->display['type:name']}", 'display-name' => $this->display['name']]
-        )[0] ?? NULL;
-      if ($afform['searchDisplay']) {
-        $this->_afform = $afform;
+      foreach ($fieldsets as $key => $fieldset) {
+        $afform['searchDisplay'] = \CRM_Utils_Array::findAll(
+            $fieldset,
+            ['#tag' => $this->display['type:name'], 'search-name' => $this->savedSearch['name'], 'display-name' => $this->display['name']]
+          )[0] ?? NULL;
+        if ($afform['searchDisplay']) {
+          // Set the fieldset for this display (if it is in one and we haven't fallen back to the whole form)
+          $afform['searchDisplay']['fieldset'] = $key === 'form' ? [] : $fieldset;
+          return $this->_afform = $afform;
+        }
       }
     }
     return $this->_afform;
diff --git a/ext/search_kit/tests/phpunit/api/v4/SearchDisplay/SearchAfformTest.php b/ext/search_kit/tests/phpunit/api/v4/SearchDisplay/SearchAfformTest.php
index 577589455467..15d5425f39c7 100644
--- a/ext/search_kit/tests/phpunit/api/v4/SearchDisplay/SearchAfformTest.php
+++ b/ext/search_kit/tests/phpunit/api/v4/SearchDisplay/SearchAfformTest.php
@@ -5,6 +5,7 @@
 use Civi\Api4\Afform;
 use Civi\Api4\Contact;
 use Civi\Api4\Email;
+use Civi\Api4\Phone;
 use Civi\Api4\SavedSearch;
 use Civi\Api4\SearchDisplay;
 use Civi\Api4\Utils\CoreUtil;
@@ -163,6 +164,175 @@ public function testRunWithAfform() {
     $this->assertCount(1, $result);
   }
 
+  public function testRunMultipleSearchForm() {
+    $email = uniqid('tester@');
+
+    Contact::create(FALSE)
+      ->addValue('first_name', 'tester')
+      ->addValue('last_name', __FUNCTION__)
+      ->addValue('source', 'afform_multi_test')
+      ->addChain('emails', Email::save()
+        ->addDefault('contact_id', '$id')
+        ->addRecord(['email' => $email, 'location_type_id:name' => 'Home'])
+        ->addRecord(['email' => $email, 'location_type_id:name' => 'Work'])
+      )
+      ->addChain('phones', Phone::save()
+        ->addDefault('contact_id', '$id')
+        ->addRecord(['phone' => '123-4567', 'location_type_id:name' => 'Home'])
+        ->addRecord(['phone' => '234-5678', 'location_type_id:name' => 'Work'])
+      )
+      ->execute();
+
+    Contact::create(FALSE)
+      ->addValue('first_name', 'tester2')
+      ->addValue('last_name', __FUNCTION__)
+      ->addValue('source', 'afform_multi_test')
+      ->addChain('emails', Email::save()
+        ->addDefault('contact_id', '$id')
+        ->addRecord(['email' => 'other@test.com', 'location_type_id:name' => 'Other'])
+      )
+      ->addChain('phones', Phone::save()
+        ->addDefault('contact_id', '$id')
+        ->addRecord(['phone' => '123-4567', 'location_type_id:name' => 'Home'])
+        ->addRecord(['phone' => '234-5678', 'location_type_id:name' => 'Work'])
+      )
+      ->execute();
+
+    // Decoy contact just to make sure we don't get false-positives
+    Contact::create(FALSE)
+      ->addValue('first_name', 'tester3')
+      ->addValue('last_name', 'nobody')
+      ->addValue('source', 'decoy')
+      ->addChain('emails', Email::save()
+        ->addDefault('contact_id', '$id')
+        ->addRecord(['email' => $email, 'location_type_id:name' => 'Home'])
+      )
+      ->addChain('phones', Phone::save()
+        ->addDefault('contact_id', '$id')
+        ->addRecord(['phone' => '123-4567', 'location_type_id:name' => 'Home'])
+        ->addRecord(['phone' => '234-5678', 'location_type_id:name' => 'Work'])
+      )
+      ->execute();
+
+    $contactEmailSearch = SavedSearch::create(FALSE)
+      ->setValues([
+        'name' => 'TestContactEmailSearch',
+        'label' => 'TestContactEmailSearch',
+        'api_entity' => 'Contact',
+        'api_params' => [
+          'version' => 4,
+          'select' => [
+            'id',
+            'display_name',
+            'GROUP_CONCAT(DISTINCT Contact_Email_contact_id_01.email) AS GROUP_CONCAT_Contact_Email_contact_id_01_email',
+          ],
+          'orderBy' => [],
+          'where' => [
+            ['contact_type:name', '=', 'Individual'],
+          ],
+          'groupBy' => ['id'],
+          'join' => [
+            [
+              'Email AS Contact_Email_contact_id_01',
+              'LEFT',
+              ['id', '=', 'Contact_Email_contact_id_01.contact_id'],
+            ],
+          ],
+          'having' => [],
+        ],
+      ])
+      ->execute()->first();
+
+    $contactEmailDisplay = SearchDisplay::create(FALSE)
+      ->setValues([
+        'name' => 'TestContactEmailDisplay',
+        'label' => 'TestContactEmailDisplay',
+        'saved_search_id.name' => 'TestContactEmailSearch',
+        'type' => 'table',
+        'settings' => [
+          'limit' => 50,
+          'pager' => TRUE,
+          'columns' => [
+            [
+              'key' => 'id',
+              'label' => 'Contact ID',
+              'dataType' => 'Integer',
+              'type' => 'field',
+            ],
+            [
+              'key' => 'display_name',
+              'label' => 'Display Name',
+              'dataType' => 'String',
+              'type' => 'field',
+            ],
+            [
+              'key' => 'GROUP_CONCAT_Contact_Email_contact_id_01_email',
+              'label' => 'Emails',
+              'dataType' => 'String',
+              'type' => 'field',
+            ],
+          ],
+        ],
+        'acl_bypass' => FALSE,
+      ])
+      ->execute()->first();
+
+    foreach (['Email', 'Phone'] as $entity) {
+      SavedSearch::create(FALSE)
+        ->setValues([
+          'name' => 'TestSearchFor' . $entity,
+          'label' => 'TestSearchFor' . $entity,
+          'api_entity' => $entity,
+          'api_params' => [
+            'version' => 4,
+            'select' => [
+              'id',
+              'contact_id.display_name',
+            ],
+            'orderBy' => [],
+            'where' => [],
+            'groupBy' => [],
+            'join' => [],
+            'having' => [],
+          ],
+        ])
+        ->execute();
+    }
+
+    $params = [
+      'return' => 'page:1',
+      'display' => NULL,
+      'afform' => 'testMultipleSearchForm',
+    ];
+
+    // This filter will not work because the search display is not within an <af-field>
+    $params['savedSearch'] = 'TestSearchForPhone';
+    $params['filters'] = ['location_type_id' => 1];
+    $result = civicrm_api4('SearchDisplay', 'run', $params);
+    $this->assertCount(4, $result);
+
+    $params['savedSearch'] = 'TestSearchForEmail';
+    $params['filters'] = ['location_type_id' => 1, 'contact_id.display_name' => __FUNCTION__];
+    $result = civicrm_api4('SearchDisplay', 'run', $params);
+    $this->assertCount(1, $result);
+
+    // Email filter will not work because it's in the wrong fieldset on the form
+    $params['filters'] = ['email' => $email, 'contact_id.display_name' => __FUNCTION__];
+    $result = civicrm_api4('SearchDisplay', 'run', $params);
+    $this->assertCount(3, $result);
+
+    // No filters will work; they are in the fieldset belonging to the non-default display
+    $params['savedSearch'] = 'TestContactEmailSearch';
+    $params['filters'] = ['source' => 'afform_multi_test', 'Contact_Email_contact_id_01.location_type_id' => 1];
+    $result = civicrm_api4('SearchDisplay', 'run', $params);
+    $this->assertGreaterThanOrEqual(3, $result->count());
+
+    // Now the filters will work because they are in the fieldset for this display
+    $params['display'] = 'TestContactEmailDisplay';
+    $result = civicrm_api4('SearchDisplay', 'run', $params);
+    $this->assertCount(1, $result);
+  }
+
   public function testSearchReferencesToAfform() {
     $search = SavedSearch::create(FALSE)
       ->setValues([