diff --git a/src/WebJobs.Script.WebHost/Security/Authentication/Jwt/ScriptJwtBearerExtensions.cs b/src/WebJobs.Script.WebHost/Security/Authentication/Jwt/ScriptJwtBearerExtensions.cs
index f8f9d692f0..3b3557bdbc 100644
--- a/src/WebJobs.Script.WebHost/Security/Authentication/Jwt/ScriptJwtBearerExtensions.cs
+++ b/src/WebJobs.Script.WebHost/Security/Authentication/Jwt/ScriptJwtBearerExtensions.cs
@@ -86,7 +86,7 @@ public static AuthenticationBuilder AddScriptJwtBearer(this AuthenticationBuilde
                             }
                         });
 
-        private static string[] GetValidAudiences()
+        private static IEnumerable<string> GetValidAudiences()
         {
             if (SystemEnvironment.Instance.IsPlaceholderModeEnabled()
                 && SystemEnvironment.Instance.IsLinuxConsumptionOnAtlas())
@@ -97,11 +97,22 @@ private static string[] GetValidAudiences()
                 };
             }
 
-            return new string[]
+            string siteName = ScriptSettingsManager.Instance.GetSetting(AzureWebsiteName);
+            string runtimeSiteName = ScriptSettingsManager.Instance.GetSetting(AzureWebsiteRuntimeSiteName);
+            var audiences = new List<string>
             {
-                string.Format(SiteAzureFunctionsUriFormat, ScriptSettingsManager.Instance.GetSetting(AzureWebsiteName)),
-                string.Format(SiteUriFormat, ScriptSettingsManager.Instance.GetSetting(AzureWebsiteName))
+                string.Format(SiteAzureFunctionsUriFormat, siteName),
+                string.Format(SiteUriFormat, siteName)
             };
+
+            if (!string.IsNullOrEmpty(runtimeSiteName) && !string.Equals(siteName, runtimeSiteName, StringComparison.OrdinalIgnoreCase))
+            {
+                // on a non-production slot, the runtime site name will differ from the site name
+                // we allow both for audience
+                audiences.Add(string.Format(SiteUriFormat, runtimeSiteName));
+            }
+
+            return audiences;
         }
 
         public static TokenValidationParameters CreateTokenValidationParameters()
diff --git a/test/WebJobs.Script.Tests/Extensions/ScriptJwtBearerExtensionsTests.cs b/test/WebJobs.Script.Tests/Extensions/ScriptJwtBearerExtensionsTests.cs
index fc8c9fdabb..7bf622e3d1 100644
--- a/test/WebJobs.Script.Tests/Extensions/ScriptJwtBearerExtensionsTests.cs
+++ b/test/WebJobs.Script.Tests/Extensions/ScriptJwtBearerExtensionsTests.cs
@@ -67,5 +67,43 @@ public void CreateTokenValidationParameters_HasExpectedAudience(bool isPlacehold
                 }
             }
         }
+
+        [Theory]
+        [InlineData("testsite", "testsite")]
+        [InlineData("testsite", "testsite__5bb5")]
+        [InlineData("testsite", null)]
+        [InlineData("testsite", "")]
+        public void CreateTokenValidationParameters_NonProductionSlot_HasExpectedAudiences(string siteName, string runtimeSiteName)
+        {
+            string azFuncAudience = string.Format(ScriptConstants.SiteAzureFunctionsUriFormat, siteName);
+            string siteAudience = string.Format(ScriptConstants.SiteUriFormat, siteName);
+            string runtimeSiteAudience = string.Format(ScriptConstants.SiteUriFormat, runtimeSiteName);
+
+            var testEnv = new Dictionary<string, string>(StringComparer.OrdinalIgnoreCase)
+            {
+                { EnvironmentSettingNames.AzureWebsiteName, siteName },
+                { EnvironmentSettingNames.AzureWebsiteRuntimeSiteName, runtimeSiteName },
+                { ContainerEncryptionKey, Convert.ToBase64String(TestHelpers.GenerateKeyBytes()) }
+            };
+
+            using (new TestScopedSettings(ScriptSettingsManager.Instance, testEnv))
+            {
+                var tokenValidationParameters = ScriptJwtBearerExtensions.CreateTokenValidationParameters();
+                var audiences = tokenValidationParameters.ValidAudiences.ToArray();
+
+                Assert.Equal(audiences[0], azFuncAudience);
+                Assert.Equal(audiences[1], siteAudience);
+
+                if (string.Compare(siteName, runtimeSiteName, StringComparison.OrdinalIgnoreCase) == 0)
+                {
+                    Assert.Equal(2, audiences.Length);
+                }
+                else if (!string.IsNullOrEmpty(runtimeSiteName))
+                {
+                    Assert.Equal(3, audiences.Length);
+                    Assert.Equal(audiences[2], runtimeSiteAudience);
+                }
+            }
+        }
     }
 }
\ No newline at end of file