diff --git a/docs/release-notes/version-2.9.md b/docs/release-notes/version-2.9.md
index 977cb08e0..3d6ad5b81 100644
--- a/docs/release-notes/version-2.9.md
+++ b/docs/release-notes/version-2.9.md
@@ -2,6 +2,10 @@
 
 ## v2.9.9 (FUTURE)
 
+### Enhancements
+
+* [#5304](https://github.com/netbox-community/netbox/issues/5304) - Return server error messages as JSON when handling REST API requests
+
 ### Bug Fixes
 
 * [#5271](https://github.com/netbox-community/netbox/issues/5271) - Fix auto-population of region field when editing a device
diff --git a/netbox/utilities/middleware.py b/netbox/utilities/middleware.py
index d86be752b..605f10e42 100644
--- a/netbox/utilities/middleware.py
+++ b/netbox/utilities/middleware.py
@@ -7,7 +7,7 @@ from django.http import Http404, HttpResponseRedirect
 from django.urls import reverse
 
 from .api import is_api_request
-from .views import server_error
+from .views import server_error, rest_api_server_error
 
 
 class LoginRequiredMiddleware(object):
@@ -86,6 +86,10 @@ class ExceptionHandlingMiddleware(object):
         if isinstance(exception, Http404):
             return
 
+        # Handle exceptions that occur from REST API requests
+        if is_api_request(request):
+            return rest_api_server_error(request)
+
         # Determine the type of exception. If it's a common issue, return a custom error page with instructions.
         custom_template = None
         if isinstance(exception, ProgrammingError):
diff --git a/netbox/utilities/views.py b/netbox/utilities/views.py
index 1dae60107..df8982755 100644
--- a/netbox/utilities/views.py
+++ b/netbox/utilities/views.py
@@ -13,7 +13,7 @@ from django.core.exceptions import FieldDoesNotExist, ImproperlyConfigured, Obje
 from django.db import transaction, IntegrityError
 from django.db.models import ManyToManyField, ProtectedError
 from django.forms import Form, ModelMultipleChoiceField, MultipleHiddenInput, Textarea
-from django.http import HttpResponse, HttpResponseServerError
+from django.http import HttpResponse, HttpResponseServerError, JsonResponse
 from django.shortcuts import get_object_or_404, redirect, render
 from django.template import loader
 from django.template.exceptions import TemplateDoesNotExist
@@ -27,6 +27,7 @@ from django.views.decorators.csrf import requires_csrf_token
 from django.views.defaults import ERROR_500_TEMPLATE_NAME
 from django.views.generic import View
 from django_tables2 import RequestConfig
+from rest_framework import status
 
 from extras.models import CustomField, CustomFieldValue, ExportTemplate
 from extras.querysets import CustomFieldQueryset
@@ -1423,8 +1424,22 @@ def server_error(request, template_name=ERROR_500_TEMPLATE_NAME):
     type_, error, traceback = sys.exc_info()
 
     return HttpResponseServerError(template.render({
-        'python_version': platform.python_version(),
-        'netbox_version': settings.VERSION,
-        'exception': str(type_),
         'error': error,
+        'exception': str(type_),
+        'netbox_version': settings.VERSION,
+        'python_version': platform.python_version(),
     }))
+
+
+def rest_api_server_error(request, *args, **kwargs):
+    """
+    Handle exceptions and return a useful error message for REST API requests.
+    """
+    type_, error, traceback = sys.exc_info()
+    data = {
+        'error': str(error),
+        'exception': type_.__name__,
+        'netbox_version': settings.VERSION,
+        'python_version': platform.python_version(),
+    }
+    return JsonResponse(data, status=status.HTTP_500_INTERNAL_SERVER_ERROR)