diff --git a/system/Debug/ExceptionHandler.php b/system/Debug/ExceptionHandler.php
index 76d5e0f2e504..805b5691c079 100644
--- a/system/Debug/ExceptionHandler.php
+++ b/system/Debug/ExceptionHandler.php
@@ -13,6 +13,7 @@
 
 namespace CodeIgniter\Debug;
 
+use Closure;
 use CodeIgniter\API\ResponseTrait;
 use CodeIgniter\Exceptions\PageNotFoundException;
 use CodeIgniter\HTTP\CLIRequest;
@@ -85,6 +86,12 @@ public function handle(
                     ? $this->collectVars($exception, $statusCode)
                     : '';
 
+                // Sanitize data to remove non-JSON-serializable values (resources, closures)
+                // before formatting for API responses (JSON, XML, etc.)
+                if ($data !== '') {
+                    $data = $this->sanitizeData($data);
+                }
+
                 $this->respond($data, $statusCode)->send();
 
                 if (ENVIRONMENT !== 'testing') {
@@ -167,4 +174,53 @@ private function isDisplayErrorsEnabled(): bool
             true,
         );
     }
+
+    /**
+     * Sanitizes data to remove non-JSON-serializable values like resources and closures.
+     * This is necessary for API responses that need to be JSON/XML encoded.
+     *
+     * @param array<int, bool> $seen Used internally to prevent infinite recursion
+     */
+    private function sanitizeData(mixed $data, array &$seen = []): mixed
+    {
+        $type = gettype($data);
+
+        switch ($type) {
+            case 'resource':
+            case 'resource (closed)':
+                return '[Resource #' . (int) $data . ']';
+
+            case 'array':
+                $result = [];
+
+                foreach ($data as $key => $value) {
+                    $result[$key] = $this->sanitizeData($value, $seen);
+                }
+
+                return $result;
+
+            case 'object':
+                $oid = spl_object_id($data);
+                if (isset($seen[$oid])) {
+                    return '[' . $data::class . ' Object *RECURSION*]';
+                }
+                $seen[$oid] = true;
+
+                if ($data instanceof Closure) {
+                    return '[Closure]';
+                }
+
+                $result = [];
+
+                foreach ((array) $data as $key => $value) {
+                    $cleanKey          = preg_replace('/^\x00.*\x00/', '', (string) $key);
+                    $result[$cleanKey] = $this->sanitizeData($value, $seen);
+                }
+
+                return $result;
+
+            default:
+                return $data;
+        }
+    }
 }
diff --git a/tests/system/Debug/ExceptionHandlerTest.php b/tests/system/Debug/ExceptionHandlerTest.php
index a278ade8be7e..a1958be5f36b 100644
--- a/tests/system/Debug/ExceptionHandlerTest.php
+++ b/tests/system/Debug/ExceptionHandlerTest.php
@@ -22,6 +22,7 @@
 use Config\Exceptions as ExceptionsConfig;
 use Config\Services;
 use PHPUnit\Framework\Attributes\Group;
+use stdClass;
 
 /**
  * @internal
@@ -262,4 +263,127 @@ public function testHighlightFile(): void
 
         $this->restoreIniValues();
     }
+
+    public function testSanitizeDataWithResource(): void
+    {
+        $sanitizeData = self::getPrivateMethodInvoker($this->handler, 'sanitizeData');
+
+        // Create a resource (file handle)
+        $resource = fopen('php://memory', 'rb');
+        $result   = $sanitizeData($resource);
+
+        $this->assertIsString($result);
+        $this->assertStringStartsWith('[Resource #', $result);
+        $this->assertStringEndsWith(']', $result);
+
+        fclose($resource);
+    }
+
+    public function testSanitizeDataWithClosure(): void
+    {
+        $sanitizeData = self::getPrivateMethodInvoker($this->handler, 'sanitizeData');
+
+        $closure = static fn (): string => 'test';
+        $result  = $sanitizeData($closure);
+
+        $this->assertSame('[Closure]', $result);
+    }
+
+    public function testSanitizeDataWithCircularReference(): void
+    {
+        $sanitizeData = self::getPrivateMethodInvoker($this->handler, 'sanitizeData');
+
+        // Create an object with circular reference
+        $obj       = new stdClass();
+        $obj->self = $obj;
+
+        $result = $sanitizeData($obj);
+
+        $this->assertIsArray($result);
+        $this->assertArrayHasKey('self', $result);
+        $this->assertStringContainsString('*RECURSION*', (string) $result['self']);
+        $this->assertStringContainsString('stdClass', (string) $result['self']);
+    }
+
+    public function testSanitizeDataWithArrayContainingResource(): void
+    {
+        $sanitizeData = self::getPrivateMethodInvoker($this->handler, 'sanitizeData');
+
+        $resource = fopen('php://memory', 'rb');
+        $data     = [
+            'string'   => 'test',
+            'number'   => 123,
+            'resource' => $resource,
+        ];
+
+        $result = $sanitizeData($data);
+
+        $this->assertIsArray($result);
+        $this->assertSame('test', $result['string']);
+        $this->assertSame(123, $result['number']);
+        $this->assertIsString($result['resource']);
+        $this->assertStringStartsWith('[Resource #', $result['resource']);
+
+        fclose($resource);
+    }
+
+    public function testSanitizeDataWithObjectContainingResource(): void
+    {
+        $sanitizeData = self::getPrivateMethodInvoker($this->handler, 'sanitizeData');
+
+        $resource = fopen('php://memory', 'rb');
+
+        $obj           = new stdClass();
+        $obj->name     = 'test';
+        $obj->connID   = $resource;
+        $obj->database = 'mydb';
+
+        $result = $sanitizeData($obj);
+
+        $this->assertIsArray($result);
+        $this->assertSame('test', $result['name']);
+        $this->assertSame('mydb', $result['database']);
+        $this->assertIsString($result['connID']);
+        $this->assertStringStartsWith('[Resource #', $result['connID']);
+
+        fclose($resource);
+    }
+
+    public function testSanitizeDataWithNestedObjects(): void
+    {
+        $sanitizeData = self::getPrivateMethodInvoker($this->handler, 'sanitizeData');
+
+        $resource = fopen('php://memory', 'rb');
+
+        $inner         = new stdClass();
+        $inner->connID = $resource;
+        $inner->host   = 'localhost';
+
+        $outer        = new stdClass();
+        $outer->db    = $inner;
+        $outer->cache = 'file';
+
+        $result = $sanitizeData($outer);
+
+        $this->assertIsArray($result);
+        $this->assertSame('file', $result['cache']);
+        $this->assertIsArray($result['db']);
+        $this->assertSame('localhost', $result['db']['host']);
+        $this->assertIsString($result['db']['connID']);
+        $this->assertStringStartsWith('[Resource #', $result['db']['connID']);
+
+        fclose($resource);
+    }
+
+    public function testSanitizeDataWithScalars(): void
+    {
+        $sanitizeData = self::getPrivateMethodInvoker($this->handler, 'sanitizeData');
+
+        $this->assertSame('string', $sanitizeData('string'));
+        $this->assertSame(123, $sanitizeData(123));
+        $this->assertEqualsWithDelta(45.67, $sanitizeData(45.67), PHP_FLOAT_EPSILON);
+        $this->assertTrue($sanitizeData(true));
+        $this->assertFalse($sanitizeData(false));
+        $this->assertNull($sanitizeData(null));
+    }
 }
diff --git a/user_guide_src/source/changelogs/v4.6.4.rst b/user_guide_src/source/changelogs/v4.6.4.rst
index c8cc53437233..edc679e5cb7b 100644
--- a/user_guide_src/source/changelogs/v4.6.4.rst
+++ b/user_guide_src/source/changelogs/v4.6.4.rst
@@ -41,6 +41,7 @@ Bugs Fixed
 - **Database:** Fixed a bug in ``Connection::getFieldData()`` for ``SQLSRV`` and ``OCI8`` where extra characters were returned in column default values (specific to those handlers), instead of following the convention used by other drivers.
 - **Database:** Fixed a bug in ``BaseBuilder::compileOrderBy()`` where the method could overwrite ``QBOrderBy`` with a string instead of keeping it as an array, causing type errors and preventing additional ``ORDER BY`` clauses from being appended.
 - **Database:** Fixed a bug in ``SQLite3`` where the password parameter was ignored unless it was an empty string.
+- **Debug:** Fixed a bug in ``ExceptionHandler`` where JSON encoding would fail when exception traces contained resources (e.g., database connections), closures, or circular references.
 - **Forge:** Fixed a bug in ``Postgre`` and ``SQLSRV`` where changing a column's default value using ``Forge::modifyColumn()`` method produced incorrect SQL syntax.
 - **Model:** Fixed a bug in ``Model::replace()`` where ``created_at`` field (when available) wasn't set correctly.
 - **Model:** Fixed a bug in ``Model::insertBatch()`` and ``Model::updateBatch()`` where casts were not applied to inserted or updated values.