diff --git a/src/Microsoft.AspNetCore.Routing/Properties/Resources.Designer.cs b/src/Microsoft.AspNetCore.Routing/Properties/Resources.Designer.cs
index 5cb82620c1..6d2bb0a7c9 100644
--- a/src/Microsoft.AspNetCore.Routing/Properties/Resources.Designer.cs
+++ b/src/Microsoft.AspNetCore.Routing/Properties/Resources.Designer.cs
@@ -249,7 +249,7 @@ namespace Microsoft.AspNetCore.Routing
             => string.Format(CultureInfo.CurrentCulture, GetString("TemplateRoute_InvalidParameterName"), p0);
 
         /// <summary>
-        /// The route template cannot start with a '/' or '~' character.
+        /// The route template cannot start with a '~' character unless followed by a '/'.
         /// </summary>
         internal static string TemplateRoute_InvalidRouteTemplate
         {
@@ -257,7 +257,7 @@ namespace Microsoft.AspNetCore.Routing
         }
 
         /// <summary>
-        /// The route template cannot start with a '/' or '~' character.
+        /// The route template cannot start with a '~' character unless followed by a '/'.
         /// </summary>
         internal static string FormatTemplateRoute_InvalidRouteTemplate()
             => GetString("TemplateRoute_InvalidRouteTemplate");
diff --git a/src/Microsoft.AspNetCore.Routing/Resources.resx b/src/Microsoft.AspNetCore.Routing/Resources.resx
index 96ecf1f445..d883906f7c 100644
--- a/src/Microsoft.AspNetCore.Routing/Resources.resx
+++ b/src/Microsoft.AspNetCore.Routing/Resources.resx
@@ -1,17 +1,17 @@
 <?xml version="1.0" encoding="utf-8"?>
 <root>
-  <!--
-    Microsoft ResX Schema
-
+  <!-- 
+    Microsoft ResX Schema 
+    
     Version 2.0
-
-    The primary goals of this format is to allow a simple XML format
-    that is mostly human readable. The generation and parsing of the
-    various data types are done through the TypeConverter classes
+    
+    The primary goals of this format is to allow a simple XML format 
+    that is mostly human readable. The generation and parsing of the 
+    various data types are done through the TypeConverter classes 
     associated with the data types.
-
+    
     Example:
-
+    
     ... ado.net/XML headers & schema ...
     <resheader name="resmimetype">text/microsoft-resx</resheader>
     <resheader name="version">2.0</resheader>
@@ -26,36 +26,36 @@
         <value>[base64 mime encoded string representing a byte array form of the .NET Framework object]</value>
         <comment>This is a comment</comment>
     </data>
-
-    There are any number of "resheader" rows that contain simple
+                
+    There are any number of "resheader" rows that contain simple 
     name/value pairs.
-
-    Each data row contains a name, and value. The row also contains a
-    type or mimetype. Type corresponds to a .NET class that support
-    text/value conversion through the TypeConverter architecture.
-    Classes that don't support this are serialized and stored with the
+    
+    Each data row contains a name, and value. The row also contains a 
+    type or mimetype. Type corresponds to a .NET class that support 
+    text/value conversion through the TypeConverter architecture. 
+    Classes that don't support this are serialized and stored with the 
     mimetype set.
-
-    The mimetype is used for serialized objects, and tells the
-    ResXResourceReader how to depersist the object. This is currently not
+    
+    The mimetype is used for serialized objects, and tells the 
+    ResXResourceReader how to depersist the object. This is currently not 
     extensible. For a given mimetype the value must be set accordingly:
-
-    Note - application/x-microsoft.net.object.binary.base64 is the format
-    that the ResXResourceWriter will generate, however the reader can
+    
+    Note - application/x-microsoft.net.object.binary.base64 is the format 
+    that the ResXResourceWriter will generate, however the reader can 
     read any of the formats listed below.
-
+    
     mimetype: application/x-microsoft.net.object.binary.base64
-    value   : The object must be serialized with
+    value   : The object must be serialized with 
             : System.Runtime.Serialization.Formatters.Binary.BinaryFormatter
             : and then encoded with base64 encoding.
-
+    
     mimetype: application/x-microsoft.net.object.soap.base64
-    value   : The object must be serialized with
+    value   : The object must be serialized with 
             : System.Runtime.Serialization.Formatters.Soap.SoapFormatter
             : and then encoded with base64 encoding.
 
     mimetype: application/x-microsoft.net.object.bytearray.base64
-    value   : The object must be serialized into a byte array
+    value   : The object must be serialized into a byte array 
             : using a System.ComponentModel.TypeConverter
             : and then encoded with base64 encoding.
     -->
@@ -169,7 +169,7 @@
     <value>The route parameter name '{0}' is invalid. Route parameter names must be non-empty and cannot contain these characters: '{{', '}}', '/'. The '?' character marks a parameter as optional, and can occur only at the end of the parameter. The '*' character marks a parameter as catch-all, and can occur only at the start of the parameter.</value>
   </data>
   <data name="TemplateRoute_InvalidRouteTemplate" xml:space="preserve">
-    <value>The route template cannot start with a '/' or '~' character.</value>
+    <value>The route template cannot start with a '~' character unless followed by a '/'.</value>
   </data>
   <data name="TemplateRoute_MismatchedParameter" xml:space="preserve">
     <value>There is an incomplete parameter in the route template. Check that each '{' character has a matching '}' character.</value>
diff --git a/src/Microsoft.AspNetCore.Routing/Template/TemplateParser.cs b/src/Microsoft.AspNetCore.Routing/Template/TemplateParser.cs
index 51f598a486..0168b22a4b 100644
--- a/src/Microsoft.AspNetCore.Routing/Template/TemplateParser.cs
+++ b/src/Microsoft.AspNetCore.Routing/Template/TemplateParser.cs
@@ -25,12 +25,9 @@ namespace Microsoft.AspNetCore.Routing.Template
                 routeTemplate = String.Empty;
             }
 
-            if (IsInvalidRouteTemplate(routeTemplate))
-            {
-                throw new ArgumentException(Resources.TemplateRoute_InvalidRouteTemplate, nameof(routeTemplate));
-            }
+            var trimmedRouteTemplate = TrimPrefix(routeTemplate);
 
-            var context = new TemplateParserContext(routeTemplate);
+            var context = new TemplateParserContext(trimmedRouteTemplate);
             var segments = new List<TemplateSegment>();
 
             while (context.Next())
@@ -61,6 +58,23 @@ namespace Microsoft.AspNetCore.Routing.Template
             }
         }
 
+        private static string TrimPrefix(string routeTemplate)
+        {
+            if (routeTemplate.StartsWith("~/", StringComparison.Ordinal))
+            {
+                return routeTemplate.Substring(2);
+            }
+            else if (routeTemplate.StartsWith("/", StringComparison.Ordinal))
+            {
+                return routeTemplate.Substring(1);
+            }
+            else if (routeTemplate.StartsWith("~", StringComparison.Ordinal))
+            {
+                throw new ArgumentException(Resources.TemplateRoute_InvalidRouteTemplate, nameof(routeTemplate));
+            }
+            return routeTemplate;
+        }
+
         private static bool ParseSegment(TemplateParserContext context, List<TemplateSegment> segments)
         {
             Debug.Assert(context != null);
diff --git a/test/Microsoft.AspNetCore.Routing.Tests/Template/TemplateBinderTests.cs b/test/Microsoft.AspNetCore.Routing.Tests/Template/TemplateBinderTests.cs
index 4d71164ce6..ab06c3f2cc 100644
--- a/test/Microsoft.AspNetCore.Routing.Tests/Template/TemplateBinderTests.cs
+++ b/test/Microsoft.AspNetCore.Routing.Tests/Template/TemplateBinderTests.cs
@@ -691,6 +691,28 @@ namespace Microsoft.AspNetCore.Routing.Template.Tests
                 "/UrlEncode[[v1]]");
         }
 
+        [Fact]
+        public void GetUrlWithLeadingTildeSlash()
+        {
+            RunTest(
+                "~/foo",
+                null,
+                null,
+                new RouteValueDictionary(new { }),
+                "/UrlEncode[[foo]]");
+        }
+
+        [Fact]
+        public void GetUrlWithLeadingSlash()
+        {
+            RunTest(
+                "/foo",
+                null,
+                null,
+                new RouteValueDictionary(new { }),
+                "/UrlEncode[[foo]]");
+        }
+
         [Fact]
         public void TemplateBinder_KeepsExplicitlySuppliedRouteValues_OnFailedRouetMatch()
         {
@@ -721,7 +743,7 @@ namespace Microsoft.AspNetCore.Routing.Template.Tests
 
 #if ROUTE_COLLECTION
 
-                [Fact]
+        [Fact]
         public void GetUrlShouldValidateOnlyAcceptedParametersAndUserDefaultValuesForInvalidatedParameters()
         {
             // Arrange
@@ -755,7 +777,7 @@ namespace Microsoft.AspNetCore.Routing.Template.Tests
             Assert.Equal<string>("/app1/UrlConstraints/Validation.mvc/Input5/MissmatchedValidateParameters2/valid1", vpd.VirtualPath);
         }
 
-               [Fact]
+        [Fact]
         public void GetUrlWithRouteThatHasExtensionWithSubsequentDefaultValueIncludesExtensionButNotDefaultValue()
         {
             // Arrange
diff --git a/test/Microsoft.AspNetCore.Routing.Tests/Template/TemplateParserTests.cs b/test/Microsoft.AspNetCore.Routing.Tests/Template/TemplateParserTests.cs
index 7ffd8f1026..7f9f9b8b40 100644
--- a/test/Microsoft.AspNetCore.Routing.Tests/Template/TemplateParserTests.cs
+++ b/test/Microsoft.AspNetCore.Routing.Tests/Template/TemplateParserTests.cs
@@ -655,6 +655,18 @@ namespace Microsoft.AspNetCore.Routing.Template.Tests
                 "Parameter name: routeTemplate");
         }
 
+        [Theory]
+        [InlineData("/foo")]
+        [InlineData("~/foo")]
+        public void ValidTemplate_CanStartWithSlashOrTildeSlash(string routeTemplate)
+        {
+            // Arrange & Act
+            var template = TemplateParser.Parse(routeTemplate);
+
+            // Assert
+            Assert.Equal(routeTemplate, template.TemplateText);
+        }
+
         [Fact]
         public void InvalidTemplate_CannotHaveConsecutiveOpenBrace()
         {
@@ -768,21 +780,12 @@ namespace Microsoft.AspNetCore.Routing.Template.Tests
                 "Parameter name: routeTemplate");
         }
 
-        [Fact]
-        public void InvalidTemplate_CannotStartWithSlash()
-        {
-            ExceptionAssert.Throws<ArgumentException>(
-                () => TemplateParser.Parse("/foo"),
-                "The route template cannot start with a '/' or '~' character." + Environment.NewLine +
-                "Parameter name: routeTemplate");
-        }
-
         [Fact]
         public void InvalidTemplate_CannotStartWithTilde()
         {
             ExceptionAssert.Throws<ArgumentException>(
                 () => TemplateParser.Parse("~foo"),
-                "The route template cannot start with a '/' or '~' character." + Environment.NewLine +
+                "The route template cannot start with a '~' character unless followed by a '/'." + Environment.NewLine +
                 "Parameter name: routeTemplate");
         }