diff --git a/src/Microsoft.AspNetCore.Mvc.RazorPages/DependencyInjection/RazorPagesOptionsExtensions.cs b/src/Microsoft.AspNetCore.Mvc.RazorPages/DependencyInjection/RazorPagesOptionsExtensions.cs
index fa8d0f142a..c7b46332db 100644
--- a/src/Microsoft.AspNetCore.Mvc.RazorPages/DependencyInjection/RazorPagesOptionsExtensions.cs
+++ b/src/Microsoft.AspNetCore.Mvc.RazorPages/DependencyInjection/RazorPagesOptionsExtensions.cs
@@ -193,9 +193,9 @@ namespace Microsoft.Extensions.DependencyInjection
                 throw new ArgumentException(Resources.ArgumentCannotBeNullOrEmpty, nameof(pageName));
             }
 
-            if (string.IsNullOrEmpty(route))
+            if (route == null)
             {
-                throw new ArgumentException(Resources.ArgumentCannotBeNullOrEmpty, nameof(route));
+                throw new ArgumentNullException(nameof(route));
             }
 
             options.Conventions.Add(new PageConvention(pageName, model =>
diff --git a/test/Microsoft.AspNetCore.Mvc.FunctionalTests/RazorPagesTest.cs b/test/Microsoft.AspNetCore.Mvc.FunctionalTests/RazorPagesTest.cs
index 196563e4cd..ac243614da 100644
--- a/test/Microsoft.AspNetCore.Mvc.FunctionalTests/RazorPagesTest.cs
+++ b/test/Microsoft.AspNetCore.Mvc.FunctionalTests/RazorPagesTest.cs
@@ -1037,6 +1037,19 @@ Microsoft.AspNetCore.Mvc.ViewFeatures.ViewDataDictionary`1[AspNetCore._InjectedP
             Assert.StartsWith(expected, response.Trim());
         }
 
+        [Fact]
+        public async Task PagesCanByRoutedToApplicationRoot_ViaAddPageRoute()
+        {
+            // Arrange
+            var expected = "Hello from NotTheRoot";
+
+            // Act
+            var response = await Client.GetStringAsync("");
+
+            // Assert
+            Assert.StartsWith(expected, response.Trim());
+        }
+
         private async Task AddAntiforgeryHeaders(HttpRequestMessage request)
         {
             var getResponse = await Client.GetAsync(request.RequestUri);
diff --git a/test/WebSites/RazorPagesWebSite/Pages/NotTheRoot.cshtml b/test/WebSites/RazorPagesWebSite/Pages/NotTheRoot.cshtml
new file mode 100644
index 0000000000..f919c9d628
--- /dev/null
+++ b/test/WebSites/RazorPagesWebSite/Pages/NotTheRoot.cshtml
@@ -0,0 +1,2 @@
+@page
+Hello from NotTheRoot
diff --git a/test/WebSites/RazorPagesWebSite/Startup.cs b/test/WebSites/RazorPagesWebSite/Startup.cs
index d4c369bfb1..04e213fdc9 100644
--- a/test/WebSites/RazorPagesWebSite/Startup.cs
+++ b/test/WebSites/RazorPagesWebSite/Startup.cs
@@ -20,6 +20,7 @@ namespace RazorPagesWebSite
                     options.AuthorizeFolder("/Pages/Admin");
                     options.AllowAnonymousToPage("/Pages/Admin/Login");
                     options.AddPageRoute("/HelloWorldWithRoute", "Different-Route/{text}");
+                    options.AddPageRoute("/Pages/NotTheRoot", string.Empty);
                 })
                 .WithRazorPagesAtContentRoot();
         }