diff --git a/netbox/dcim/tests/test_api.py b/netbox/dcim/tests/test_api.py
index 8b6cac98d..c70b546e3 100644
--- a/netbox/dcim/tests/test_api.py
+++ b/netbox/dcim/tests/test_api.py
@@ -13,7 +13,8 @@ from ipam.choices import VLANQinQRoleChoices
 from ipam.models import ASN, RIR, VLAN, VRF
 from netbox.api.serializers import GenericObjectSerializer
 from tenancy.models import Tenant
-from users.models import User
+from users.constants import TOKEN_PREFIX
+from users.models import Token, User
 from utilities.testing import APITestCase, APIViewTestCases, create_test_device, disable_logging
 from virtualization.models import Cluster, ClusterType
 from wireless.choices import WirelessChannelChoices
@@ -1485,8 +1486,8 @@ class DeviceTest(APIViewTestCases.APIViewTestCase):
         device.config_template = configtemplate
         device.save()
 
-        self.add_permissions('dcim.render_config_device', 'dcim.view_device', 'extras.view_configtemplate')
-        url = reverse('dcim-api:device-detail', kwargs={'pk': device.pk}) + 'render-config/'
+        self.add_permissions('dcim.render_config_device', 'dcim.view_device')
+        url = reverse('dcim-api:device-render-config', kwargs={'pk': device.pk})
         response = self.client.post(url, {}, format='json', **self.header)
         self.assertHttpStatus(response, status.HTTP_200_OK)
         self.assertEqual(response.data['content'], f'Config for device {device.name}')
@@ -1502,10 +1503,41 @@ class DeviceTest(APIViewTestCases.APIViewTestCase):
         device.save()
 
         # No permissions added - user has no render_config permission
-        url = reverse('dcim-api:device-detail', kwargs={'pk': device.pk}) + 'render-config/'
+        url = reverse('dcim-api:device-render-config', kwargs={'pk': device.pk})
         response = self.client.post(url, {}, format='json', **self.header)
         self.assertHttpStatus(response, status.HTTP_404_NOT_FOUND)
 
+    def test_render_config_token_write_enabled(self):
+        configtemplate = ConfigTemplate.objects.create(
+            name='Config Template 1',
+            template_code='Config for device {{ device.name }}'
+        )
+
+        device = Device.objects.first()
+        device.config_template = configtemplate
+        device.save()
+
+        self.add_permissions('dcim.render_config_device', 'dcim.view_device')
+        url = reverse('dcim-api:device-render-config', kwargs={'pk': device.pk})
+
+        # Request without token auth should fail with PermissionDenied
+        response = self.client.post(url, {}, format='json')
+        self.assertHttpStatus(response, status.HTTP_403_FORBIDDEN)
+
+        # Create token with write_enabled=False
+        token = Token.objects.create(version=2, user=self.user, write_enabled=False)
+        token_header = f'Bearer {TOKEN_PREFIX}{token.key}.{token.token}'
+
+        # Request with write-disabled token should fail
+        response = self.client.post(url, {}, format='json', HTTP_AUTHORIZATION=token_header)
+        self.assertHttpStatus(response, status.HTTP_403_FORBIDDEN)
+
+        # Enable write and retry
+        token.write_enabled = True
+        token.save()
+        response = self.client.post(url, {}, format='json', HTTP_AUTHORIZATION=token_header)
+        self.assertHttpStatus(response, status.HTTP_200_OK)
+
 
 class ModuleTest(APIViewTestCases.APIViewTestCase):
     model = Module
diff --git a/netbox/extras/api/mixins.py b/netbox/extras/api/mixins.py
index 0716788f7..7a15364f7 100644
--- a/netbox/extras/api/mixins.py
+++ b/netbox/extras/api/mixins.py
@@ -1,7 +1,5 @@
-from django.utils.translation import gettext_lazy as _
 from jinja2.exceptions import TemplateError
 from rest_framework.decorators import action
-from rest_framework.exceptions import PermissionDenied
 from rest_framework.renderers import JSONRenderer
 from rest_framework.response import Response
 from rest_framework.status import HTTP_400_BAD_REQUEST
@@ -91,10 +89,6 @@ class RenderConfigMixin(ConfigTemplateRenderMixin):
                 'error': f'No config template found for this {object_type}.'
             }, status=HTTP_400_BAD_REQUEST)
 
-        # Check view permission for ConfigTemplate
-        if not request.user.has_perm('extras.view_configtemplate', obj=configtemplate):
-            raise PermissionDenied(_("This user does not have permission to view this configuration template."))
-
         # Compile context data
         context_data = instance.get_config_context()
         context_data.update(request.data)
diff --git a/netbox/extras/tests/test_api.py b/netbox/extras/tests/test_api.py
index ea55668ca..92cdd88bd 100644
--- a/netbox/extras/tests/test_api.py
+++ b/netbox/extras/tests/test_api.py
@@ -12,7 +12,8 @@ from dcim.models import Device, DeviceRole, DeviceType, Manufacturer, Rack, Loca
 from extras.choices import *
 from extras.models import *
 from extras.scripts import BooleanVar, IntegerVar, Script as PythonClass, StringVar
-from users.models import Group, User
+from users.constants import TOKEN_PREFIX
+from users.models import Group, Token, User
 from utilities.testing import APITestCase, APIViewTestCases
 
 
@@ -859,7 +860,7 @@ class ConfigTemplateTest(APIViewTestCases.APIViewTestCase):
         configtemplate = ConfigTemplate.objects.first()
 
         self.add_permissions('extras.render_configtemplate', 'extras.view_configtemplate')
-        url = reverse('extras-api:configtemplate-detail', kwargs={'pk': configtemplate.pk}) + 'render/'
+        url = reverse('extras-api:configtemplate-render', kwargs={'pk': configtemplate.pk})
         response = self.client.post(url, {'foo': 'bar'}, format='json', **self.header)
         self.assertHttpStatus(response, status.HTTP_200_OK)
         self.assertEqual(response.data['content'], 'Foo: bar')
@@ -868,10 +869,34 @@ class ConfigTemplateTest(APIViewTestCases.APIViewTestCase):
         configtemplate = ConfigTemplate.objects.first()
 
         # No permissions added - user has no render permission
-        url = reverse('extras-api:configtemplate-detail', kwargs={'pk': configtemplate.pk}) + 'render/'
+        url = reverse('extras-api:configtemplate-render', kwargs={'pk': configtemplate.pk})
         response = self.client.post(url, {'foo': 'bar'}, format='json', **self.header)
         self.assertHttpStatus(response, status.HTTP_404_NOT_FOUND)
 
+    def test_render_token_write_enabled(self):
+        configtemplate = ConfigTemplate.objects.first()
+
+        self.add_permissions('extras.render_configtemplate', 'extras.view_configtemplate')
+        url = reverse('extras-api:configtemplate-render', kwargs={'pk': configtemplate.pk})
+
+        # Request without token auth should fail with PermissionDenied
+        response = self.client.post(url, {'foo': 'bar'}, format='json')
+        self.assertHttpStatus(response, status.HTTP_403_FORBIDDEN)
+
+        # Create token with write_enabled=False
+        token = Token.objects.create(version=2, user=self.user, write_enabled=False)
+        token_header = f'Bearer {TOKEN_PREFIX}{token.key}.{token.token}'
+
+        # Request with write-disabled token should fail
+        response = self.client.post(url, {'foo': 'bar'}, format='json', HTTP_AUTHORIZATION=token_header)
+        self.assertHttpStatus(response, status.HTTP_403_FORBIDDEN)
+
+        # Enable write and retry
+        token.write_enabled = True
+        token.save()
+        response = self.client.post(url, {'foo': 'bar'}, format='json', HTTP_AUTHORIZATION=token_header)
+        self.assertHttpStatus(response, status.HTTP_200_OK)
+
 
 class ScriptTest(APITestCase):
 
diff --git a/netbox/netbox/api/authentication.py b/netbox/netbox/api/authentication.py
index 7397f99ba..7dbc38598 100644
--- a/netbox/netbox/api/authentication.py
+++ b/netbox/netbox/api/authentication.py
@@ -169,10 +169,13 @@ class TokenWritePermission(BasePermission):
     Verify the token has write_enabled for unsafe methods, without requiring specific model permissions.
     Used for custom actions that accept user data but don't map to standard CRUD operations.
     """
+
     def has_permission(self, request, view):
-        if isinstance(request.auth, Token):
-            return request.method in SAFE_METHODS or request.auth.write_enabled
-        return True
+        if not isinstance(request.auth, Token):
+            raise exceptions.PermissionDenied(
+                "TokenWritePermission requires token authentication."
+            )
+        return bool(request.method in SAFE_METHODS or request.auth.write_enabled)
 
 
 class IsAuthenticatedOrLoginNotRequired(BasePermission):
diff --git a/netbox/virtualization/tests/test_api.py b/netbox/virtualization/tests/test_api.py
index 4c4d9be4d..56f9132ab 100644
--- a/netbox/virtualization/tests/test_api.py
+++ b/netbox/virtualization/tests/test_api.py
@@ -12,6 +12,8 @@ from extras.choices import CustomFieldTypeChoices
 from extras.models import ConfigTemplate, CustomField
 from ipam.choices import VLANQinQRoleChoices
 from ipam.models import Prefix, VLAN, VRF
+from users.constants import TOKEN_PREFIX
+from users.models import Token
 from utilities.testing import (
     APITestCase, APIViewTestCases, create_test_device, create_test_virtualmachine, disable_logging,
 )
@@ -282,10 +284,9 @@ class VirtualMachineTest(APIViewTestCases.APIViewTestCase):
         vm.save()
 
         self.add_permissions(
-            'virtualization.render_config_virtualmachine', 'virtualization.view_virtualmachine',
-            'extras.view_configtemplate'
+            'virtualization.render_config_virtualmachine', 'virtualization.view_virtualmachine'
         )
-        url = reverse('virtualization-api:virtualmachine-detail', kwargs={'pk': vm.pk}) + 'render-config/'
+        url = reverse('virtualization-api:virtualmachine-render-config', kwargs={'pk': vm.pk})
         response = self.client.post(url, {}, format='json', **self.header)
         self.assertHttpStatus(response, status.HTTP_200_OK)
         self.assertEqual(response.data['content'], f'Config for virtual machine {vm.name}')
@@ -301,10 +302,41 @@ class VirtualMachineTest(APIViewTestCases.APIViewTestCase):
         vm.save()
 
         # No permissions added - user has no render_config permission
-        url = reverse('virtualization-api:virtualmachine-detail', kwargs={'pk': vm.pk}) + 'render-config/'
+        url = reverse('virtualization-api:virtualmachine-render-config', kwargs={'pk': vm.pk})
         response = self.client.post(url, {}, format='json', **self.header)
         self.assertHttpStatus(response, status.HTTP_404_NOT_FOUND)
 
+    def test_render_config_token_write_enabled(self):
+        configtemplate = ConfigTemplate.objects.create(
+            name='Config Template 1',
+            template_code='Config for virtual machine {{ virtualmachine.name }}'
+        )
+
+        vm = VirtualMachine.objects.first()
+        vm.config_template = configtemplate
+        vm.save()
+
+        self.add_permissions('virtualization.render_config_virtualmachine', 'virtualization.view_virtualmachine')
+        url = reverse('virtualization-api:virtualmachine-render-config', kwargs={'pk': vm.pk})
+
+        # Request without token auth should fail with PermissionDenied
+        response = self.client.post(url, {}, format='json')
+        self.assertHttpStatus(response, status.HTTP_403_FORBIDDEN)
+
+        # Create token with write_enabled=False
+        token = Token.objects.create(version=2, user=self.user, write_enabled=False)
+        token_header = f'Bearer {TOKEN_PREFIX}{token.key}.{token.token}'
+
+        # Request with write-disabled token should fail
+        response = self.client.post(url, {}, format='json', HTTP_AUTHORIZATION=token_header)
+        self.assertHttpStatus(response, status.HTTP_403_FORBIDDEN)
+
+        # Enable write and retry
+        token.write_enabled = True
+        token.save()
+        response = self.client.post(url, {}, format='json', HTTP_AUTHORIZATION=token_header)
+        self.assertHttpStatus(response, status.HTTP_200_OK)
+
 
 class VMInterfaceTest(APIViewTestCases.APIViewTestCase):
     model = VMInterface