diff --git a/src/Hosting/TestHost/src/ClientHandler.cs b/src/Hosting/TestHost/src/ClientHandler.cs
index 95788035ea..06f0189aea 100644
--- a/src/Hosting/TestHost/src/ClientHandler.cs
+++ b/src/Hosting/TestHost/src/ClientHandler.cs
@@ -14,6 +14,7 @@ using System.Threading.Tasks;
 using Microsoft.AspNetCore.Hosting.Server;
 using Microsoft.AspNetCore.Http;
 using Microsoft.AspNetCore.Http.Features;
+using Microsoft.Net.Http.Headers;
 
 namespace Microsoft.AspNetCore.TestHost
 {
@@ -111,7 +112,15 @@ namespace Microsoft.AspNetCore.TestHost
 
                 foreach (var header in request.Headers)
                 {
-                    req.Headers.Append(header.Key, header.Value.ToArray());
+                    // User-Agent is a space delineated single line header but HttpRequestHeaders parses it as multiple elements.
+                    if (string.Equals(header.Key, HeaderNames.UserAgent, StringComparison.OrdinalIgnoreCase))
+                    {
+                        req.Headers.Append(header.Key, string.Join(" ", header.Value));
+                    }
+                    else
+                    {
+                        req.Headers.Append(header.Key, header.Value.ToArray());
+                    }
                 }
 
                 if (!req.Host.HasValue)
diff --git a/src/Hosting/TestHost/test/ClientHandlerTests.cs b/src/Hosting/TestHost/test/ClientHandlerTests.cs
index 521a056e15..9013b07f44 100644
--- a/src/Hosting/TestHost/test/ClientHandlerTests.cs
+++ b/src/Hosting/TestHost/test/ClientHandlerTests.cs
@@ -14,6 +14,7 @@ using Microsoft.AspNetCore.Http;
 using Microsoft.AspNetCore.Http.Features;
 using Microsoft.Extensions.DependencyInjection;
 using Microsoft.Extensions.Logging;
+using Microsoft.Net.Http.Headers;
 using Xunit;
 
 namespace Microsoft.AspNetCore.TestHost
@@ -85,6 +86,23 @@ namespace Microsoft.AspNetCore.TestHost
             return httpClient.GetAsync("https://example.com/");
         }
 
+        [Fact]
+        public Task UserAgentHeaderWorks()
+        {
+            var userAgent = "Mozilla/5.0 (Windows NT 10.0; Win64; x64; rv:71.0) Gecko/20100101 Firefox/71.0";
+            var handler = new ClientHandler(new PathString(""), new DummyApplication(context =>
+            {
+                var actualResult = context.Request.Headers[HeaderNames.UserAgent];
+                Assert.Equal(userAgent, actualResult);
+
+                return Task.CompletedTask;
+            }));
+            var httpClient = new HttpClient(handler);
+            httpClient.DefaultRequestHeaders.Add(HeaderNames.UserAgent, userAgent);
+
+            return httpClient.GetAsync("http://example.com");
+        }
+
         [Fact]
         public async Task ServerTrailersSetOnResponseAfterContentRead()
         {
diff --git a/src/Hosting/TestHost/test/HttpContextBuilderTests.cs b/src/Hosting/TestHost/test/HttpContextBuilderTests.cs
index b4731e1572..cc4570b0e3 100644
--- a/src/Hosting/TestHost/test/HttpContextBuilderTests.cs
+++ b/src/Hosting/TestHost/test/HttpContextBuilderTests.cs
@@ -12,6 +12,7 @@ using Microsoft.AspNetCore.Http;
 using Microsoft.AspNetCore.Http.Features;
 using Microsoft.Extensions.DependencyInjection;
 using Microsoft.Extensions.Logging;
+using Microsoft.Net.Http.Headers;
 using Xunit;
 
 namespace Microsoft.AspNetCore.TestHost
@@ -47,6 +48,22 @@ namespace Microsoft.AspNetCore.TestHost
             Assert.Null(context.Features.Get<IHttpResponseFeature>().ReasonPhrase);
         }
 
+        [Fact]
+        public async Task UserAgentHeaderWorks()
+        {
+            var userAgent = "Mozilla/5.0 (Windows NT 10.0; Win64; x64; rv:71.0) Gecko/20100101 Firefox/71.0";
+            var builder = new WebHostBuilder().Configure(app => { });
+            var server = new TestServer(builder);
+            server.BaseAddress = new Uri("https://example.com/");
+            var context = await server.SendAsync(c =>
+            {
+                c.Request.Headers[HeaderNames.UserAgent] = userAgent;
+            });
+
+            var actualResult = context.Request.Headers[HeaderNames.UserAgent];
+            Assert.Equal(userAgent, actualResult);
+        }
+
         [Fact]
         public async Task SingleSlashNotMovedToPathBase()
         {