diff --git a/src/Microsoft.AspNetCore.SystemWebAdapters.CoreServices/Authentication/RemoteAppAuthenticationClientOptions.cs b/src/Microsoft.AspNetCore.SystemWebAdapters.CoreServices/Authentication/RemoteAppAuthenticationClientOptions.cs
index 0efd829c51..ba43f00084 100644
--- a/src/Microsoft.AspNetCore.SystemWebAdapters.CoreServices/Authentication/RemoteAppAuthenticationClientOptions.cs
+++ b/src/Microsoft.AspNetCore.SystemWebAdapters.CoreServices/Authentication/RemoteAppAuthenticationClientOptions.cs
@@ -41,5 +41,11 @@ public class RemoteAppAuthenticationClientOptions : AuthenticationSchemeOptions
     /// services. Requests to authenticate are sent to this endpoint.
     /// </summary>
     [Required]
-    public PathString AuthenticationEndpointPath { get; set; } = AuthenticationConstants.DefaultEndpoint;
+    public PathString AuthenticationEndpointPath
+    {
+        get => Path.Path;
+        set => Path = new(value);
+    }
+
+    internal RelativePathString Path { get; private set; } = new(AuthenticationConstants.DefaultEndpoint);
 }
diff --git a/src/Microsoft.AspNetCore.SystemWebAdapters.CoreServices/Authentication/RemoteAppAuthenticationService.cs b/src/Microsoft.AspNetCore.SystemWebAdapters.CoreServices/Authentication/RemoteAppAuthenticationService.cs
index b422bb0a58..1796302772 100644
--- a/src/Microsoft.AspNetCore.SystemWebAdapters.CoreServices/Authentication/RemoteAppAuthenticationService.cs
+++ b/src/Microsoft.AspNetCore.SystemWebAdapters.CoreServices/Authentication/RemoteAppAuthenticationService.cs
@@ -85,7 +85,7 @@ public async Task<RemoteAppAuthenticationResult> AuthenticateAsync(HttpRequest o
         // that may matter for authentication. Also include the original request path as
         // as a query parameter so that the ASP.NET app can redirect back to it if an
         // authentication provider attempts to redirect back to the authenticate URL.
-        var url = $"{_options.AuthenticationEndpointPath}?{AuthenticationConstants.OriginalUrlQueryParamName}={WebUtility.UrlEncode(originalRequest.GetEncodedPathAndQuery())}";
+        var url = $"{_options.Path.Relative}?{AuthenticationConstants.OriginalUrlQueryParamName}={WebUtility.UrlEncode(originalRequest.GetEncodedPathAndQuery())}";
         using var authRequest = new HttpRequestMessage(HttpMethod.Get, url);
         AddHeaders(_options.RequestHeadersToForward, originalRequest, authRequest);
 
diff --git a/src/Microsoft.AspNetCore.SystemWebAdapters.CoreServices/RelativePathString.cs b/src/Microsoft.AspNetCore.SystemWebAdapters.CoreServices/RelativePathString.cs
new file mode 100644
index 0000000000..e87731fdae
--- /dev/null
+++ b/src/Microsoft.AspNetCore.SystemWebAdapters.CoreServices/RelativePathString.cs
@@ -0,0 +1,22 @@
+// Licensed to the .NET Foundation under one or more agreements.
+// The .NET Foundation licenses this file to you under the MIT license.
+
+using Microsoft.AspNetCore.Http;
+
+namespace Microsoft.AspNetCore.SystemWebAdapters;
+
+internal readonly struct RelativePathString
+{
+    public RelativePathString(PathString path)
+    {
+        Path = path;
+        Relative = "." + path;
+    }
+
+    public PathString Path { get; }
+
+    /// <summary>
+    /// Use when you want the path to be relative to whatever URI you may combine it with
+    /// </summary>
+    public string Relative { get; }
+}
diff --git a/src/Microsoft.AspNetCore.SystemWebAdapters.CoreServices/RemoteAppClientOptions.cs b/src/Microsoft.AspNetCore.SystemWebAdapters.CoreServices/RemoteAppClientOptions.cs
index a08dac34dd..ee4e5674cb 100644
--- a/src/Microsoft.AspNetCore.SystemWebAdapters.CoreServices/RemoteAppClientOptions.cs
+++ b/src/Microsoft.AspNetCore.SystemWebAdapters.CoreServices/RemoteAppClientOptions.cs
@@ -12,6 +12,8 @@ namespace Microsoft.AspNetCore.SystemWebAdapters;
 /// </summary>
 public class RemoteAppClientOptions
 {
+    private Uri _remoteAppUrl = null!;
+
     /// <summary>
     /// Gets or sets the header used to store the API key
     /// </summary>
@@ -28,7 +30,27 @@ public class RemoteAppClientOptions
     /// Gets or sets the remote app url
     /// </summary>
     [Required]
-    public Uri RemoteAppUrl { get; set; } = null!;
+    public Uri RemoteAppUrl
+    {
+        get => _remoteAppUrl;
+        set
+        {
+            if (value is null)
+            {
+                throw new ArgumentNullException(nameof(RemoteAppUrl));
+            }
+
+            // Path must end in '/' so that it will combine correctly with subpaths
+            if (!value.AbsolutePath.EndsWith("/"))
+            {
+                var builder = new UriBuilder(value);
+                builder.Path += "/";
+                value = builder.Uri;
+            }
+
+            _remoteAppUrl = value;
+        }
+    }
 
     /// <summary>
     /// Gets or sets an <see cref="HttpMessageHandler"/> to use for making requests to the remote app.
diff --git a/src/Microsoft.AspNetCore.SystemWebAdapters.CoreServices/SessionState/RemoteSession/RemoteAppSessionStateClientOptions.cs b/src/Microsoft.AspNetCore.SystemWebAdapters.CoreServices/SessionState/RemoteSession/RemoteAppSessionStateClientOptions.cs
index f2b7159a59..34ed3a5034 100644
--- a/src/Microsoft.AspNetCore.SystemWebAdapters.CoreServices/SessionState/RemoteSession/RemoteAppSessionStateClientOptions.cs
+++ b/src/Microsoft.AspNetCore.SystemWebAdapters.CoreServices/SessionState/RemoteSession/RemoteAppSessionStateClientOptions.cs
@@ -2,13 +2,20 @@
 // The .NET Foundation licenses this file to you under the MIT license.
 
 using System.ComponentModel.DataAnnotations;
+using Microsoft.AspNetCore.Http;
 
 namespace Microsoft.AspNetCore.SystemWebAdapters.SessionState.RemoteSession;
 
 public class RemoteAppSessionStateClientOptions
 {
     [Required]
-    public string SessionEndpointPath { get; set; } = SessionConstants.SessionEndpointPath;
+    public PathString SessionEndpointPath
+    {
+        get => Path.Path;
+        set => Path = new(value);
+    }
+
+    internal RelativePathString Path { get; private set; } = new(SessionConstants.SessionEndpointPath);
 
     /// <summary>
     /// Gets or sets the cookie name that the ASP.NET framework app is expecting to hold the session id
diff --git a/src/Microsoft.AspNetCore.SystemWebAdapters.CoreServices/SessionState/RemoteSession/RemoteAppSessionStateManager.cs b/src/Microsoft.AspNetCore.SystemWebAdapters.CoreServices/SessionState/RemoteSession/RemoteAppSessionStateManager.cs
index 4095231af3..fdaea50d42 100644
--- a/src/Microsoft.AspNetCore.SystemWebAdapters.CoreServices/SessionState/RemoteSession/RemoteAppSessionStateManager.cs
+++ b/src/Microsoft.AspNetCore.SystemWebAdapters.CoreServices/SessionState/RemoteSession/RemoteAppSessionStateManager.cs
@@ -73,7 +73,7 @@ private async Task<ISessionState> GetSessionDataAsync(string? sessionId, bool re
     {
         // The request message is manually disposed at a later time
 #pragma warning disable CA2000 // Dispose objects before losing scope
-        var req = new HttpRequestMessage(HttpMethod.Get, _options.SessionEndpointPath);
+        var req = new HttpRequestMessage(HttpMethod.Get, _options.Path.Relative);
 #pragma warning restore CA2000 // Dispose objects before losing scope
 
         AddSessionCookieToHeader(req, sessionId);
@@ -112,7 +112,7 @@ private async Task<ISessionState> GetSessionDataAsync(string? sessionId, bool re
     /// </summary>
     private async Task SetOrReleaseSessionData(ISessionState? state, CancellationToken cancellationToken)
     {
-        using var req = new HttpRequestMessage(HttpMethod.Put, _options.SessionEndpointPath);
+        using var req = new HttpRequestMessage(HttpMethod.Put, _options.Path.Relative);
 
         if (state is not null)
         {
diff --git a/src/Microsoft.AspNetCore.SystemWebAdapters.FrameworkServices/RemoteModule.cs b/src/Microsoft.AspNetCore.SystemWebAdapters.FrameworkServices/RemoteModule.cs
index 4781652e98..518e28177c 100644
--- a/src/Microsoft.AspNetCore.SystemWebAdapters.FrameworkServices/RemoteModule.cs
+++ b/src/Microsoft.AspNetCore.SystemWebAdapters.FrameworkServices/RemoteModule.cs
@@ -50,11 +50,14 @@ void IHttpModule.Dispose()
 
     void IHttpModule.Init(HttpApplication context)
     {
+        var appRelativePath = $"~{Path}";
+
         context.PostMapRequestHandler += (s, _) =>
         {
             var context = ((HttpApplication)s).Context;
 
-            if (!string.Equals(context.Request.Path, Path, StringComparison.Ordinal))
+            // Compare against the AppRelativeCurrentExecutionFilePath to account for potential virtual directories
+            if (!string.Equals(context.Request.AppRelativeCurrentExecutionFilePath, appRelativePath, StringComparison.Ordinal))
             {
                 return;
             }
diff --git a/test/Microsoft.AspNetCore.SystemWebAdapters.CoreServices.Tests/RemoteAppClientOptionsTests.cs b/test/Microsoft.AspNetCore.SystemWebAdapters.CoreServices.Tests/RemoteAppClientOptionsTests.cs
index ec7c8a1a41..c6f8771019 100644
--- a/test/Microsoft.AspNetCore.SystemWebAdapters.CoreServices.Tests/RemoteAppClientOptionsTests.cs
+++ b/test/Microsoft.AspNetCore.SystemWebAdapters.CoreServices.Tests/RemoteAppClientOptionsTests.cs
@@ -35,7 +35,11 @@ public void VerifyIsCalled(string apiKeyHeader, string apiKey, string remoteAppU
             {
                 options.ApiKey = apiKey;
                 options.ApiKeyHeader = apiKeyHeader;
-                options.RemoteAppUrl = (remoteAppUrl is null ? null : new Uri(remoteAppUrl, UriKind.Absolute))!;
+
+                if (remoteAppUrl is not null)
+                {
+                    options.RemoteAppUrl = new Uri(remoteAppUrl, UriKind.Absolute);
+                }
             }));
 
         using var serviceProvider = services.BuildServiceProvider();