diff --git a/Slim/Handlers/ErrorHandler.php b/Slim/Handlers/ErrorHandler.php
index a6b99ceac..95fa4c6d3 100644
--- a/Slim/Handlers/ErrorHandler.php
+++ b/Slim/Handlers/ErrorHandler.php
@@ -78,6 +78,8 @@ class ErrorHandler implements ErrorHandlerInterface
 
     protected ?string $contentType = null;
 
+    protected bool $isContentTypeForced = false;
+
     protected ?string $method = null;
 
     protected ServerRequestInterface $request;
@@ -125,7 +127,7 @@ public function __invoke(
         $this->exception = $exception;
         $this->method = $request->getMethod();
         $this->statusCode = $this->determineStatusCode();
-        if ($this->contentType === null) {
+        if (!$this->isContentTypeForced) {
             $this->contentType = $this->determineContentType($request);
         }
 
@@ -139,10 +141,11 @@ public function __invoke(
     /**
      * Force the content type for all error handler responses.
      *
-     * @param string|null $contentType The content type
+     * @param string|null $contentType The content type. Null restores Accept-header negotiation.
      */
     public function forceContentType(?string $contentType): void
     {
+        $this->isContentTypeForced = $contentType !== null;
         $this->contentType = $contentType;
     }
 
diff --git a/tests/Handlers/ErrorHandlerTest.php b/tests/Handlers/ErrorHandlerTest.php
index 1cd6bcc89..515673c78 100644
--- a/tests/Handlers/ErrorHandlerTest.php
+++ b/tests/Handlers/ErrorHandlerTest.php
@@ -118,6 +118,101 @@ public function testForceContentType()
         $this->assertSame(['application/json'], $response->getHeader('Content-Type'));
     }
 
+    /**
+     * Test that the content type is negotiated from the Accept header on each
+     * request instead of being cached from the first invocation.
+     */
+    public function testContentTypeIsNegotiatedOnEachRequest()
+    {
+        $handler = new ErrorHandler($this->getCallableResolver(), $this->getResponseFactory());
+
+        $jsonRequest = $this
+            ->createServerRequest('/not-defined', 'GET')
+            ->withHeader('Accept', 'application/json');
+
+        $htmlRequest = $this
+            ->createServerRequest('/not-defined', 'GET')
+            ->withHeader('Accept', 'text/html');
+
+        $exception = new HttpNotFoundException($jsonRequest);
+
+        /** @var ResponseInterface $response */
+        $response = $handler->__invoke($jsonRequest, $exception, false, false, false);
+        $this->assertSame(['application/json'], $response->getHeader('Content-Type'));
+
+        $exception = new HttpNotFoundException($htmlRequest);
+
+        /** @var ResponseInterface $response */
+        $response = $handler->__invoke($htmlRequest, $exception, false, false, false);
+        $this->assertSame(['text/html'], $response->getHeader('Content-Type'));
+    }
+
+    /**
+     * Test that a forced content type still wins over per-request negotiation.
+     */
+    public function testForcedContentTypeWinsOverSubsequentNegotiation()
+    {
+        $handler = new ErrorHandler($this->getCallableResolver(), $this->getResponseFactory());
+        $handler->forceContentType('application/json');
+
+        $jsonRequest = $this
+            ->createServerRequest('/not-defined', 'GET')
+            ->withHeader('Accept', 'application/json');
+
+        $xmlRequest = $this
+            ->createServerRequest('/not-defined', 'GET')
+            ->withHeader('Accept', 'application/xml');
+
+        $exception = new HttpNotFoundException($jsonRequest);
+
+        /** @var ResponseInterface $response */
+        $response = $handler->__invoke($jsonRequest, $exception, false, false, false);
+        $this->assertSame(['application/json'], $response->getHeader('Content-Type'));
+
+        $exception = new HttpNotFoundException($xmlRequest);
+
+        /** @var ResponseInterface $response */
+        $response = $handler->__invoke($xmlRequest, $exception, false, false, false);
+        $this->assertSame(['application/json'], $response->getHeader('Content-Type'));
+    }
+
+    /**
+     * Test that forceContentType(null) restores Accept-header negotiation.
+     */
+    public function testForceContentTypeNullRestoresNegotiation()
+    {
+        $handler = new ErrorHandler($this->getCallableResolver(), $this->getResponseFactory());
+        $handler->forceContentType('application/json');
+
+        $xmlRequest = $this
+            ->createServerRequest('/not-defined', 'GET')
+            ->withHeader('Accept', 'application/xml');
+
+        $htmlRequest = $this
+            ->createServerRequest('/not-defined', 'GET')
+            ->withHeader('Accept', 'text/html');
+
+        $exception = new HttpNotFoundException($xmlRequest);
+
+        /** @var ResponseInterface $response */
+        $response = $handler->__invoke($xmlRequest, $exception, false, false, false);
+        $this->assertSame(['application/json'], $response->getHeader('Content-Type'));
+
+        $handler->forceContentType(null);
+
+        $exception = new HttpNotFoundException($xmlRequest);
+
+        /** @var ResponseInterface $response */
+        $response = $handler->__invoke($xmlRequest, $exception, false, false, false);
+        $this->assertSame(['application/xml'], $response->getHeader('Content-Type'));
+
+        $exception = new HttpNotFoundException($htmlRequest);
+
+        /** @var ResponseInterface $response */
+        $response = $handler->__invoke($htmlRequest, $exception, false, false, false);
+        $this->assertSame(['text/html'], $response->getHeader('Content-Type'));
+    }
+
     public function testHalfValidContentType()
     {
         $request = $this