diff --git a/src/Components/test/E2ETest/Tests/SignalRClientTest.cs b/src/Components/test/E2ETest/Tests/SignalRClientTest.cs
index 9265abfc1e1f..82e313f2cd76 100644
--- a/src/Components/test/E2ETest/Tests/SignalRClientTest.cs
+++ b/src/Components/test/E2ETest/Tests/SignalRClientTest.cs
@@ -66,5 +66,21 @@ public void SignalRClientWorksWithWebSockets()
             Browser.Equal("SignalR Client: Echo WebSockets",
                 () => Browser.FindElements(By.CssSelector("li")).FirstOrDefault()?.Text);
         }
+
+        [Fact]
+        public void SignalRClientSendsUserAgent()
+        {
+            Browser.Exists(By.Id("hub-url")).SendKeys(
+                new Uri(_apiServerFixture.RootUri, "/subdir/chathub").AbsoluteUri);
+            var target = new SelectElement(Browser.Exists(By.Id("transport-type")));
+            target.SelectByText("LongPolling");
+            Browser.Exists(By.Id("hub-connect")).Click();
+
+            Browser.Equal("SignalR Client: Echo LongPolling",
+                () => Browser.FindElements(By.CssSelector("li")).FirstOrDefault()?.Text);
+
+            Browser.Exists(By.Id("hub-useragent")).Click();
+            Assert.NotNull(Browser.FindElement(By.Id("useragent")).Text);
+        }
     }
 }
diff --git a/src/Components/test/testassets/BasicTestApp/SignalRClientComponent.razor b/src/Components/test/testassets/BasicTestApp/SignalRClientComponent.razor
index a8fae272ab21..dd3a39833169 100644
--- a/src/Components/test/testassets/BasicTestApp/SignalRClientComponent.razor
+++ b/src/Components/test/testassets/BasicTestApp/SignalRClientComponent.razor
@@ -13,9 +13,11 @@
         <option value=@HttpTransportType.WebSockets>WebSockets</option>
     </select>
     <button id="hub-connect" @onclick="Connect">Connect</button>
+    <button id="hub-useragent" @onclick="GetUserAgentHeader">GetUserAgent</button>
 </p>
 
 <div>Connected: @IsConnected</div>
+<div id="useragent">User-Agent: @userAgent</div>
 
 <ul id="messagesList">
     @foreach (var message in messages)
@@ -29,6 +31,7 @@
     private HttpTransportType transportType;
     private HubConnection hubConnection;
     private List<string> messages = new List<string>();
+    private string userAgent;
 
     protected async Task Connect()
     {
@@ -47,6 +50,12 @@
         await hubConnection.SendAsync("SendMessage", "SignalR Client", $"Echo {transportType}");
     }
 
+    protected async Task GetUserAgentHeader()
+    {
+        userAgent = await hubConnection.InvokeAsync<string>("GetHeaderValue", "X-SignalR-User-Agent");
+        StateHasChanged();
+    }
+
     public bool IsConnected =>
         hubConnection != null && hubConnection.State == HubConnectionState.Connected;
 
diff --git a/src/Components/test/testassets/TestServer/ChatHub.cs b/src/Components/test/testassets/TestServer/ChatHub.cs
index 770f2dcaa9f4..eaef0eb927a3 100644
--- a/src/Components/test/testassets/TestServer/ChatHub.cs
+++ b/src/Components/test/testassets/TestServer/ChatHub.cs
@@ -1,6 +1,7 @@
 // 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;
 using System.Threading.Tasks;
 using Microsoft.AspNetCore.SignalR;
 
@@ -12,5 +13,25 @@ public async Task SendMessage(string user, string message)
         {
             await Clients.All.SendAsync("ReceiveMessage", user, message);
         }
+
+        public string GetHeaderValue(string headerName)
+        {
+            var context = Context.GetHttpContext();
+
+            if (context == null)
+            {
+                throw new InvalidOperationException("Unable to get HttpContext from request.");
+            }
+
+            var headers = context.Request.Headers;
+
+            if (headers == null)
+            {
+                throw new InvalidOperationException("Unable to get headers from context.");
+            }
+
+            headers.TryGetValue(headerName, out var val);
+            return val.ToString();
+        }
     }
 }
diff --git a/src/SignalR/clients/csharp/Http.Connections.Client/src/HttpConnection.cs b/src/SignalR/clients/csharp/Http.Connections.Client/src/HttpConnection.cs
index 6bd1cd88fdee..bb0f786db1df 100644
--- a/src/SignalR/clients/csharp/Http.Connections.Client/src/HttpConnection.cs
+++ b/src/SignalR/clients/csharp/Http.Connections.Client/src/HttpConnection.cs
@@ -597,8 +597,7 @@ private HttpClient CreateHttpClient()
             var httpClient = new HttpClient(httpMessageHandler);
             httpClient.Timeout = HttpClientTimeout;
 
-            // Start with the user agent header
-            httpClient.DefaultRequestHeaders.Add(Constants.UserAgent, Constants.UserAgentHeader);
+            var userSetUserAgent = false;
 
             // Apply any headers configured on the HttpConnectionOptions
             if (_httpConnectionOptions?.Headers != null)
@@ -608,6 +607,7 @@ private HttpClient CreateHttpClient()
                     // Check if the key is User-Agent and remove if empty string then replace if it exists.
                     if (string.Equals(header.Key, Constants.UserAgent, StringComparison.OrdinalIgnoreCase))
                     {
+                        userSetUserAgent = true;
                         if (string.IsNullOrEmpty(header.Value))
                         {
                             httpClient.DefaultRequestHeaders.Remove(header.Key);
@@ -629,6 +629,14 @@ private HttpClient CreateHttpClient()
                 }
             }
 
+            // Apply default user agent only if user hasn't specified one (empty or not)
+            // Don't pre-emptively set this, some frameworks (mono) have different user agent format rules,
+            // so allowing a user to set an empty one avoids throwing on those frameworks.
+            if (!userSetUserAgent)
+            {
+                httpClient.DefaultRequestHeaders.Add(Constants.UserAgent, Constants.UserAgentHeader);
+            }
+
             httpClient.DefaultRequestHeaders.Remove("X-Requested-With");
             // Tell auth middleware to 401 instead of redirecting
             httpClient.DefaultRequestHeaders.Add("X-Requested-With", "XMLHttpRequest");
diff --git a/src/SignalR/clients/csharp/Http.Connections.Client/src/Internal/Constants.cs b/src/SignalR/clients/csharp/Http.Connections.Client/src/Internal/Constants.cs
index 862772a2a492..ed6687834944 100644
--- a/src/SignalR/clients/csharp/Http.Connections.Client/src/Internal/Constants.cs
+++ b/src/SignalR/clients/csharp/Http.Connections.Client/src/Internal/Constants.cs
@@ -11,11 +11,16 @@ namespace Microsoft.AspNetCore.Http.Connections.Client.Internal
 {
     internal static class Constants
     {
-        public const string UserAgent = "User-Agent";
+        public static readonly string UserAgent = "User-Agent";
         public static readonly string UserAgentHeader;
 
         static Constants()
         {
+            if (OperatingSystem.IsBrowser())
+            {
+                UserAgent = "X-SignalR-User-Agent";
+            }
+
             var assemblyVersion = typeof(Constants)
                 .Assembly
                 .GetCustomAttributes<AssemblyInformationalVersionAttribute>()