diff --git a/src/Hosting/Abstractions/src/HostingAbstractionsWebHostBuilderExtensions.cs b/src/Hosting/Abstractions/src/HostingAbstractionsWebHostBuilderExtensions.cs
index f61b86eb86..1aac2e31d1 100644
--- a/src/Hosting/Abstractions/src/HostingAbstractionsWebHostBuilderExtensions.cs
+++ b/src/Hosting/Abstractions/src/HostingAbstractionsWebHostBuilderExtensions.cs
@@ -23,7 +23,7 @@ namespace Microsoft.AspNetCore.Hosting
         /// <returns>The <see cref="IWebHostBuilder"/>.</returns>
         public static IWebHostBuilder UseConfiguration(this IWebHostBuilder hostBuilder, IConfiguration configuration)
         {
-            foreach (var setting in configuration.AsEnumerable())
+            foreach (var setting in configuration.AsEnumerable(makePathsRelative: true))
             {
                 hostBuilder.UseSetting(setting.Key, setting.Value);
             }
diff --git a/src/Hosting/Hosting/test/WebHostBuilderTests.cs b/src/Hosting/Hosting/test/WebHostBuilderTests.cs
index 876959ddb4..5a9f280340 100644
--- a/src/Hosting/Hosting/test/WebHostBuilderTests.cs
+++ b/src/Hosting/Hosting/test/WebHostBuilderTests.cs
@@ -1,4 +1,4 @@
-// Copyright (c) .NET Foundation. All rights reserved.
+// Copyright (c) .NET Foundation. All rights reserved.
 // Licensed under the Apache License, Version 2.0. See License.txt in the project root for license information.
 
 using System;
@@ -1129,6 +1129,33 @@ namespace Microsoft.AspNetCore.Hosting
             Assert.Contains("No application configured.", exception.Message);
         }
 
+        [Theory]
+        [MemberData(nameof(DefaultWebHostBuildersWithConfig))]
+        public void UseConfigurationWithSectionAddsSubKeys(IWebHostBuilder builder)
+        {
+            var config = new ConfigurationBuilder()
+                .AddInMemoryCollection(new[]
+                {
+                    new KeyValuePair<string, string>("key", "value"),
+                    new KeyValuePair<string, string>("nested:key", "nestedvalue"),
+                }).Build();
+            var section = config.GetSection("nested");
+
+            builder = builder
+                .CaptureStartupErrors(false)
+                .Configure(app => { })
+                .UseConfiguration(section)
+                .UseServer(new TestServer());
+
+            Assert.Equal("nestedvalue", builder.GetSetting("key"));
+
+            using (var host = builder.Build())
+            {
+                var appConfig = host.Services.GetRequiredService<IConfiguration>();
+                Assert.Equal("nestedvalue", appConfig["key"]);
+            }
+        }
+
         private static void StaticConfigureMethod(IApplicationBuilder app) { }
 
         private IWebHostBuilder CreateWebHostBuilder()