diff --git a/src/Microsoft.AspNetCore.Mvc.RazorPages/Internal/PageRouteModelFactory.cs b/src/Microsoft.AspNetCore.Mvc.RazorPages/Internal/PageRouteModelFactory.cs
index 0b75e6a22d..682d55141f 100644
--- a/src/Microsoft.AspNetCore.Mvc.RazorPages/Internal/PageRouteModelFactory.cs
+++ b/src/Microsoft.AspNetCore.Mvc.RazorPages/Internal/PageRouteModelFactory.cs
@@ -60,21 +60,15 @@ namespace Microsoft.AspNetCore.Mvc.RazorPages.Internal
         {
             model.RouteValues.Add("page", model.ViewEnginePath);
 
-            if (AttributeRouteModel.IsOverridePattern(routeTemplate))
-            {
-                throw new InvalidOperationException(string.Format(
-                    Resources.PageActionDescriptorProvider_RouteTemplateCannotBeOverrideable,
-                    model.RelativePath));
-            }
-
             var selectorModel = CreateSelectorModel(pageRoute, routeTemplate);
             model.Selectors.Add(selectorModel);
 
             var fileName = Path.GetFileName(model.RelativePath);
-            if (string.Equals(IndexFileName, fileName, StringComparison.OrdinalIgnoreCase))
+            if (!AttributeRouteModel.IsOverridePattern(routeTemplate) &&
+                string.Equals(IndexFileName, fileName, StringComparison.OrdinalIgnoreCase))
             {
-                // For pages ending in /Index.cshtml, we want to allow incoming routing, but
-                // force outgoing routes to match to the path sans /Index.
+                // For pages without an override route, and ending in /Index.cshtml, we want to allow 
+                // incoming routing, but force outgoing routes to match to the path sans /Index.
                 selectorModel.AttributeRouteModel.SuppressLinkGeneration = true;
 
                 var index = pageRoute.LastIndexOf('/');
diff --git a/src/Microsoft.AspNetCore.Mvc.RazorPages/Resources.resx b/src/Microsoft.AspNetCore.Mvc.RazorPages/Resources.resx
index be0f94f186..90e0ea9300 100644
--- a/src/Microsoft.AspNetCore.Mvc.RazorPages/Resources.resx
+++ b/src/Microsoft.AspNetCore.Mvc.RazorPages/Resources.resx
@@ -117,9 +117,6 @@
   <resheader name="writer">
     <value>System.Resources.ResXResourceWriter, System.Windows.Forms, Version=4.0.0.0, Culture=neutral, PublicKeyToken=b77a5c561934e089</value>
   </resheader>
-  <data name="PageActionDescriptorProvider_RouteTemplateCannotBeOverrideable" xml:space="preserve">
-    <value>The route for the page at '{0}' cannot start with / or ~/. Pages do not support overriding the file path of the page.</value>
-  </data>
   <data name="PropertyOfTypeCannotBeNull" xml:space="preserve">
     <value>The '{0}' property of '{1}' must not be null.</value>
   </data>
diff --git a/test/Microsoft.AspNetCore.Mvc.FunctionalTests/RazorPagesTest.cs b/test/Microsoft.AspNetCore.Mvc.FunctionalTests/RazorPagesTest.cs
index 856e88cb94..ea36e1bb7c 100644
--- a/test/Microsoft.AspNetCore.Mvc.FunctionalTests/RazorPagesTest.cs
+++ b/test/Microsoft.AspNetCore.Mvc.FunctionalTests/RazorPagesTest.cs
@@ -1233,6 +1233,16 @@ Microsoft.AspNetCore.Mvc.ViewFeatures.ViewDataDictionary`1[AspNetCore.InjectedPa
             Assert.Equal(HttpStatusCode.Redirect, response.StatusCode);
         }
 
+        [Fact]
+        public async Task Page_CanOverrideRouteTemplate()
+        {
+            // Arrange & Act
+            var content = await Client.GetStringAsync("like-totally-custom");
+
+            // Assert
+            Assert.Equal("<p>Hey, it's Mr. totally custom here!</p>", content.Trim());
+        }
+
         private async Task AddAntiforgeryHeaders(HttpRequestMessage request)
         {
             var getResponse = await Client.GetAsync(request.RequestUri);
diff --git a/test/Microsoft.AspNetCore.Mvc.RazorPages.Test/Internal/CompiledPageRouteModelProviderTest.cs b/test/Microsoft.AspNetCore.Mvc.RazorPages.Test/Internal/CompiledPageRouteModelProviderTest.cs
index 011681f152..b270ee3389 100644
--- a/test/Microsoft.AspNetCore.Mvc.RazorPages.Test/Internal/CompiledPageRouteModelProviderTest.cs
+++ b/test/Microsoft.AspNetCore.Mvc.RazorPages.Test/Internal/CompiledPageRouteModelProviderTest.cs
@@ -479,23 +479,40 @@ namespace Microsoft.AspNetCore.Mvc.RazorPages.Internal
         }
 
         [Fact]
-        public void OnProvidersExecuting_ThrowsIfRouteTemplateHasOverridePattern()
+        public void OnProvidersExecuting_AllowsRouteTemplatesWithOverridePattern()
         {
             // Arrange
             var descriptors = new[]
             {
-                CreateVersion_2_0_Descriptor("/Pages/Index.cshtml"),
+                CreateVersion_2_0_Descriptor("/Pages/Index.cshtml", "~/some-other-prefix"),
                 CreateVersion_2_0_Descriptor("/Pages/Home.cshtml", "/some-prefix"),
             };
 
             var provider = CreateProvider(descriptors: descriptors);
             var context = new PageRouteModelProviderContext();
 
-            // Act & Assert
-            var exception = Assert.Throws<InvalidOperationException>(() => provider.OnProvidersExecuting(context));
-            Assert.Equal(
-                "The route for the page at '/Pages/Home.cshtml' cannot start with / or ~/. Pages do not support overriding the file path of the page.",
-                exception.Message);
+            // Act
+            provider.OnProvidersExecuting(context);
+
+            // Assert
+            Assert.Collection(
+                context.RouteModels,
+                result =>
+                {
+                    Assert.Equal("/Pages/Index.cshtml", result.RelativePath);
+                    Assert.Equal("/Index", result.ViewEnginePath);
+                    Assert.Collection(
+                        result.Selectors,
+                        selector => Assert.Equal("some-other-prefix", selector.AttributeRouteModel.Template));
+                },
+                result =>
+                {
+                    Assert.Equal("/Pages/Home.cshtml", result.RelativePath);
+                    Assert.Equal("/Home", result.ViewEnginePath);
+                    Assert.Collection(
+                        result.Selectors,
+                        selector => Assert.Equal("some-prefix", selector.AttributeRouteModel.Template));
+                });
         }
 
         private TestCompiledPageRouteModelProvider CreateProvider(
diff --git a/test/Microsoft.AspNetCore.Mvc.RazorPages.Test/Internal/PageRouteModelFactoryTest.cs b/test/Microsoft.AspNetCore.Mvc.RazorPages.Test/Internal/PageRouteModelFactoryTest.cs
index 7e8aeeb734..67bb226d06 100644
--- a/test/Microsoft.AspNetCore.Mvc.RazorPages.Test/Internal/PageRouteModelFactoryTest.cs
+++ b/test/Microsoft.AspNetCore.Mvc.RazorPages.Test/Internal/PageRouteModelFactoryTest.cs
@@ -67,6 +67,34 @@ namespace Microsoft.AspNetCore.Mvc.RazorPages.Internal
                 });
         }
 
+        [Fact]
+        public void CreateRouteModel_DoesNotAddMultipleSelectorsWhenRouteTemplateIsAbsolute()
+        {
+            // Arrange
+            var relativePath = "/Pages/Users/Profile/Index.cshtml";
+            var options = new RazorPagesOptions();
+            var routeModelFactory = new PageRouteModelFactory(options, NullLogger.Instance);
+
+            // Act
+            var routeModel = routeModelFactory.CreateRouteModel(relativePath, "/my-override");
+
+            // Assert
+            Assert.Equal(relativePath, routeModel.RelativePath);
+            Assert.Equal("/Users/Profile/Index", routeModel.ViewEnginePath);
+
+            Assert.Collection(
+                routeModel.Selectors,
+                selector => Assert.Equal("my-override", selector.AttributeRouteModel.Template));
+
+            Assert.Collection(
+                routeModel.RouteValues,
+                kvp =>
+                {
+                    Assert.Equal("page", kvp.Key);
+                    Assert.Equal("/Users/Profile/Index", kvp.Value);
+                });
+        }
+
         [Fact]
         public void CreateAreaRouteModel_AddsSelector()
         {
diff --git a/test/Microsoft.AspNetCore.Mvc.RazorPages.Test/Internal/RazorProjectPageRouteModelProviderTest.cs b/test/Microsoft.AspNetCore.Mvc.RazorPages.Test/Internal/RazorProjectPageRouteModelProviderTest.cs
index 37fd8c6ac6..8054e21a4f 100644
--- a/test/Microsoft.AspNetCore.Mvc.RazorPages.Test/Internal/RazorProjectPageRouteModelProviderTest.cs
+++ b/test/Microsoft.AspNetCore.Mvc.RazorPages.Test/Internal/RazorProjectPageRouteModelProviderTest.cs
@@ -282,7 +282,7 @@ namespace Microsoft.AspNetCore.Mvc.RazorPages.Internal
         }
 
         [Fact]
-        public void OnProvidersExecuting_ThrowsIfRouteTemplateHasOverridePattern()
+        public void OnProvidersExecuting_AllowsRouteTemplateWithOverridePattern()
         {
             // Arrange
             var fileProvider = new TestFileProvider();
@@ -296,10 +296,20 @@ namespace Microsoft.AspNetCore.Mvc.RazorPages.Internal
             var provider = new RazorProjectPageRouteModelProvider(project, optionsManager, NullLoggerFactory.Instance);
             var context = new PageRouteModelProviderContext();
 
-            // Act & Assert
-            var ex = Assert.Throws<InvalidOperationException>(() => provider.OnProvidersExecuting(context));
-            Assert.Equal("The route for the page at '/Index.cshtml' cannot start with / or ~/. Pages do not support overriding the file path of the page.",
-                ex.Message);
+            // Act
+            provider.OnProvidersExecuting(context);
+
+            // Assert
+            Assert.Collection(
+                context.RouteModels,
+                model =>
+                {
+                    Assert.Equal("/Index.cshtml", model.RelativePath);
+                    Assert.Equal("/Index", model.ViewEnginePath);
+                    Assert.Collection(
+                        model.Selectors,
+                        selector => Assert.Equal("custom-route", selector.AttributeRouteModel.Template));
+                });
         }
 
         [Fact]
diff --git a/test/WebSites/RazorPagesWebSite/Pages/CustomPrefix/Custom.cshtml b/test/WebSites/RazorPagesWebSite/Pages/CustomPrefix/Custom.cshtml
new file mode 100644
index 0000000000..ace20dc097
--- /dev/null
+++ b/test/WebSites/RazorPagesWebSite/Pages/CustomPrefix/Custom.cshtml
@@ -0,0 +1,3 @@
+@page "~/like-totally-custom"
+
+<p>Hey, it's Mr. totally custom here!</p>