diff --git a/src/base/EagerLoadingFieldInterface.php b/src/base/EagerLoadingFieldInterface.php
index 38d5fb2d06a..9005f3e6658 100644
--- a/src/base/EagerLoadingFieldInterface.php
+++ b/src/base/EagerLoadingFieldInterface.php
@@ -13,7 +13,7 @@
  * @author Pixel & Tonic, Inc. <support@pixelandtonic.com>
  * @since 3.0.0
  */
-interface EagerLoadingFieldInterface
+interface EagerLoadingFieldInterface extends FieldInterface
 {
     /**
      * Returns an array that maps source-to-target element IDs based on this custom field.
diff --git a/src/base/GqlInlineFragmentFieldInterface.php b/src/base/GqlInlineFragmentFieldInterface.php
index 6d3fc183475..ffdbf6bddb9 100644
--- a/src/base/GqlInlineFragmentFieldInterface.php
+++ b/src/base/GqlInlineFragmentFieldInterface.php
@@ -13,7 +13,7 @@
  * @author Pixel & Tonic, Inc. <support@pixelandtonic.com>
  * @since 3.3.0
  */
-interface GqlInlineFragmentFieldInterface
+interface GqlInlineFragmentFieldInterface extends FieldInterface
 {
     /**
      * Returns a GraphQL fragment by its GraphQL fragment name.
diff --git a/src/elements/db/ElementQuery.php b/src/elements/db/ElementQuery.php
index 5877d7c7227..32cd461fd55 100644
--- a/src/elements/db/ElementQuery.php
+++ b/src/elements/db/ElementQuery.php
@@ -132,6 +132,7 @@ class ElementQuery extends Query implements ElementQueryInterface
 
     /**
      * @var FieldInterface[]|null The fields that may be involved in this query.
+     * @todo make this private in v6
      */
     public ?array $customFields = null;
 
@@ -1437,6 +1438,19 @@ public function anyStatus(): static
     // Query preparation/execution
     // -------------------------------------------------------------------------
 
+    /**
+     * Returns the custom fields that may be involved in this query.
+     *
+     * @since 5.5.0
+     */
+    public function getCustomFields(): array
+    {
+        if (!isset($this->customFields)) {
+            $this->customFields = $this->customFields();
+        }
+        return $this->customFields;
+    }
+
     /**
      * @inheritdoc
      */
diff --git a/src/gql/ElementQueryConditionBuilder.php b/src/gql/ElementQueryConditionBuilder.php
index 289e4bfccfd..509c702f42c 100644
--- a/src/gql/ElementQueryConditionBuilder.php
+++ b/src/gql/ElementQueryConditionBuilder.php
@@ -37,6 +37,7 @@
 use GraphQL\Language\AST\VariableNode;
 use GraphQL\Type\Definition\ResolveInfo;
 use GraphQL\Type\Definition\WrappingType;
+use Illuminate\Support\Arr;
 use yii\base\InvalidArgumentException;
 
 /**
@@ -83,8 +84,13 @@ class ElementQueryConditionBuilder extends Component
      */
     private ArgumentManager $_argumentManager;
 
+    /**
+     * @var FieldInterface[]
+     * @see setCustomFields()
+     */
+    private array $_fields = [];
+
     private array $_fragments;
-    private array $_eagerLoadableFieldsByContext = [];
     private array $_transformableAssetProperties = ['url', 'width', 'height'];
     private array $_additionalEagerLoadableNodes;
 
@@ -102,15 +108,6 @@ public function __construct($config = [])
         }
 
         parent::__construct($config);
-
-        // Cache all eager-loadable fields by context
-        $allFields = Craft::$app->getFields()->getAllFields(false);
-
-        foreach ($allFields as $field) {
-            if ($field instanceof EagerLoadingFieldInterface) {
-                $this->_eagerLoadableFieldsByContext[$field->context][$field->handle] = $field;
-            }
-        }
     }
 
     /**
@@ -135,6 +132,17 @@ public function setArgumentManager(ArgumentManager $argumentManager): void
         $this->_argumentManager = $argumentManager;
     }
 
+    /**
+     * Sets the custom fields that may be involved in the query.
+     *
+     * @param FieldInterface[] $fields
+     * @since 5.5.0
+     */
+    public function setCustomFields(array $fields): void
+    {
+        $this->_fields = $fields;
+    }
+
     /**
      * Extract the query conditions based on the resolve information passed in the constructor.
      * Returns an array of [methodName => parameters] to be called on the element query.
@@ -410,7 +418,7 @@ private function _traversAndBuildPlans(Node $parentNode, EagerLoadPlan $parentPl
             // If that's a GraphQL field
             if ($subNode instanceof FieldNode) {
                 /** @var FieldInterface|null $craftContentField */
-                $craftContentField = $this->_eagerLoadableFieldsByContext[$context][$nodeName] ?? null;
+                $craftContentField = Arr::first($this->_fields, fn(FieldInterface $field) => $field->handle === $nodeName);
 
                 $transformableAssetProperty = ($rootOfAssetQuery || $parentField instanceof AssetField) && in_array($nodeName, $this->_transformableAssetProperties, true);
                 $isAssetField = $craftContentField instanceof AssetField;
diff --git a/src/gql/base/ElementResolver.php b/src/gql/base/ElementResolver.php
index f5455d2e4d1..fd1c64f030c 100644
--- a/src/gql/base/ElementResolver.php
+++ b/src/gql/base/ElementResolver.php
@@ -10,6 +10,7 @@
 use Craft;
 use craft\base\EagerLoadingFieldInterface;
 use craft\base\ElementInterface;
+use craft\base\FieldInterface;
 use craft\base\GqlInlineFragmentFieldInterface;
 use craft\elements\db\ElementQuery;
 use craft\elements\ElementCollection;
@@ -17,6 +18,7 @@
 use craft\gql\ElementQueryConditionBuilder;
 use craft\helpers\Gql as GqlHelper;
 use GraphQL\Type\Definition\ResolveInfo;
+use Illuminate\Support\Arr;
 
 /**
  * Class ElementResolver
@@ -92,15 +94,18 @@ protected static function prepareElementQuery(mixed $source, array $arguments, ?
             return $query;
         }
 
+        $fields = $query->getCustomFields();
         $parentField = null;
 
         if ($source instanceof ElementInterface) {
-            $fieldContext = $source->getFieldContext();
-            $field = Craft::$app->getFields()->getFieldByHandle($fieldName, $fieldContext);
+            $field = Arr::first($fields, fn(FieldInterface $field) => $field->handle === $fieldName);
 
             // This will happen if something is either dynamically added or is inside an block element that didn't support eager-loading
             // and broke the eager-loading chain. In this case Craft has to provide the relevant context so the condition knows where it's at.
-            if (($fieldContext !== 'global' && $field instanceof GqlInlineFragmentFieldInterface) || $field instanceof EagerLoadingFieldInterface) {
+            if (
+                ($source->getFieldContext() !== 'global' && $field instanceof GqlInlineFragmentFieldInterface) ||
+                $field instanceof EagerLoadingFieldInterface
+            ) {
                 $parentField = $field;
             }
         }
@@ -109,6 +114,7 @@ protected static function prepareElementQuery(mixed $source, array $arguments, ?
         $conditionBuilder = empty($context['conditionBuilder']) ? Craft::createObject(['class' => ElementQueryConditionBuilder::class]) : $context['conditionBuilder'];
         $conditionBuilder->setResolveInfo($resolveInfo);
         $conditionBuilder->setArgumentManager($argumentManager);
+        $conditionBuilder->setCustomFields($fields);
 
         $conditions = $conditionBuilder->extractQueryConditions($parentField);