diff --git a/.github/workflows/main.yml b/.github/workflows/main.yml
index d6c2b968bb..c1f87134f9 100644
--- a/.github/workflows/main.yml
+++ b/.github/workflows/main.yml
@@ -68,6 +68,7 @@ jobs:
       shell: bash
       run: |
         vstest.console /TestAdapterPath:test /Settings:test/test.runsettings \
+          test/GitHub.Api.UnitTests/bin/${{ env.config }}/net46/GitHub.Api.UnitTests.dll \
           test/GitHub.App.UnitTests/bin/${{ env.config }}/net46/GitHub.App.UnitTests.dll \
           test/GitHub.Exports.Reactive.UnitTests/bin/${{ env.config }}/net46/GitHub.Exports.Reactive.UnitTests.dll \
           test/GitHub.Exports.UnitTests/bin/${{ env.config }}/net46/GitHub.Exports.UnitTests.dll \
diff --git a/src/GitHub.Api/LoginManager.cs b/src/GitHub.Api/LoginManager.cs
index 228daa65ef..bdfe84c2c9 100644
--- a/src/GitHub.Api/LoginManager.cs
+++ b/src/GitHub.Api/LoginManager.cs
@@ -346,9 +346,14 @@ async Task<LoginResult> GetUserAndCheckScopes(IGitHubClient client)
             var response = await client.Connection.Get<User>(
                 UserEndpoint, null, null).ConfigureAwait(false);
 
-            if (response.HttpResponse.Headers.ContainsKey(ScopesHeader))
+            var scopes = response.HttpResponse.Headers
+                .Where(h => string.Equals(h.Key, ScopesHeader, StringComparison.OrdinalIgnoreCase))
+                .Select(h => h.Value)
+                .FirstOrDefault();
+
+            if (scopes != null)
             {
-                var returnedScopes = new ScopesCollection(response.HttpResponse.Headers[ScopesHeader]
+                var returnedScopes = new ScopesCollection(scopes
                     .Split(',')
                     .Select(x => x.Trim())
                     .ToArray());
diff --git a/src/GitHub.Exports/ExceptionExtensions.cs b/src/GitHub.Exports/ExceptionExtensions.cs
index a9f54c6eff..4afbb3011a 100644
--- a/src/GitHub.Exports/ExceptionExtensions.cs
+++ b/src/GitHub.Exports/ExceptionExtensions.cs
@@ -1,4 +1,5 @@
 using System;
+using System.Linq;
 using Octokit;
 
 namespace GitHub.Extensions
@@ -9,8 +10,7 @@ public static class ApiExceptionExtensions
         public static bool IsGitHubApiException(this Exception ex)
         {
             var apiex = ex as ApiException;
-            return apiex?.HttpResponse?.Headers.ContainsKey(GithubHeader) ?? false;
+            return apiex?.HttpResponse?.Headers.Keys.Contains(GithubHeader, StringComparer.OrdinalIgnoreCase) ?? false;
         }
     }
-
 }
diff --git a/submodules/octokit.net b/submodules/octokit.net
index a51818a7e0..a25a399ab7 160000
--- a/submodules/octokit.net
+++ b/submodules/octokit.net
@@ -1 +1 @@
-Subproject commit a51818a7e0879ae21aacbbfd48e62dcb172d68b4
+Subproject commit a25a399ab7994ff1cc230dac0cc07e31f3fafd1f
diff --git a/test/GitHub.Api.UnitTests/LoginManagerTests.cs b/test/GitHub.Api.UnitTests/LoginManagerTests.cs
index 6e7ca4c31c..2a2fc732be 100644
--- a/test/GitHub.Api.UnitTests/LoginManagerTests.cs
+++ b/test/GitHub.Api.UnitTests/LoginManagerTests.cs
@@ -298,13 +298,30 @@ public void InvalidResponseScopesCauseException()
             Assert.ThrowsAsync<IncorrectScopesException>(() => target.Login(host, client, "foo", "bar"));
         }
 
-        IGitHubClient CreateClient(User user = null, string[] responseScopes = null)
+        [TestCase("X-OAuth-Scopes")]
+        [TestCase("x-oauth-scopes")]
+        public void ValidResponseScopesDoesNotThrow(string scopesHeader)
+        {
+            var client = CreateClient(responseScopes: scopes, scopesHeader: scopesHeader);
+            client.Authorization.GetOrCreateApplicationAuthentication("id", "secret", Arg.Any<NewAuthorization>())
+                .Returns(CreateApplicationAuthorization("123abc"));
+
+            var keychain = Substitute.For<IKeychain>();
+            var tfa = new Lazy<ITwoFactorChallengeHandler>(() => Substitute.For<ITwoFactorChallengeHandler>());
+            var oauthListener = Substitute.For<IOAuthCallbackListener>();
+
+            var target = new LoginManager(keychain, tfa, oauthListener, "id", "secret", scopes, scopes);
+
+            Assert.DoesNotThrowAsync(() => target.Login(host, client, "foo", "bar"));
+        }
+
+        IGitHubClient CreateClient(User user = null, string[] responseScopes = null, string scopesHeader = "X-OAuth-Scopes")
         {
             var result = Substitute.For<IGitHubClient>();
             var userResponse = Substitute.For<IApiResponse<User>>();
             userResponse.HttpResponse.Headers.Returns(new Dictionary<string, string>
             {
-                {  "X-OAuth-Scopes", string.Join(",", responseScopes ?? scopes) }
+                {  scopesHeader, string.Join(",", responseScopes ?? scopes) }
             });
             userResponse.Body.Returns(user ?? new User());
             result.Connection.Get<User>(new Uri("user", UriKind.Relative), null, null).Returns(userResponse);
diff --git a/test/GitHub.Exports.UnitTests/ApiExceptionExtensionsTests.cs b/test/GitHub.Exports.UnitTests/ApiExceptionExtensionsTests.cs
new file mode 100644
index 0000000000..90133a3673
--- /dev/null
+++ b/test/GitHub.Exports.UnitTests/ApiExceptionExtensionsTests.cs
@@ -0,0 +1,42 @@
+using System.Collections.Generic;
+using System.Collections.Immutable;
+using Octokit;
+using NSubstitute;
+using NUnit.Framework;
+using GitHub.Extensions;
+
+public class ApiExceptionExtensionsTests
+{
+    public class TheIsGitHubApiExceptionMethod
+    {
+        [TestCase("Not-GitHub-Request-Id", false)]
+        [TestCase("X-GitHub-Request-Id", true)]
+        [TestCase("x-github-request-id", true)]
+        public void NoGitHubRequestId(string key, bool expect)
+        {
+            var ex = CreateApiException(new Dictionary<string, string> { { key, "ANYTHING" } });
+
+            var result = ApiExceptionExtensions.IsGitHubApiException(ex);
+
+            Assert.That(result, Is.EqualTo(expect));
+        }
+        
+        [Test]
+        public void NoResponse()
+        {
+            var ex = new ApiException();
+
+            var result = ApiExceptionExtensions.IsGitHubApiException(ex);
+
+            Assert.That(result, Is.EqualTo(false));
+        }
+
+        static ApiException CreateApiException(Dictionary<string, string> headers)
+        {
+            var response = Substitute.For<IResponse>();
+            response.Headers.Returns(headers.ToImmutableDictionary());
+            var ex = new ApiException(response);
+            return ex;
+        }
+    }
+}