diff --git a/src/Umbraco.Cms.Api.Common/DependencyInjection/ProcessRequestContextHandler.cs b/src/Umbraco.Cms.Api.Common/DependencyInjection/ProcessRequestContextHandler.cs
new file mode 100644
index 0000000000..c680ab6b34
--- /dev/null
+++ b/src/Umbraco.Cms.Api.Common/DependencyInjection/ProcessRequestContextHandler.cs
@@ -0,0 +1,53 @@
+using Microsoft.AspNetCore.Http;
+using OpenIddict.Server;
+using OpenIddict.Validation;
+using Umbraco.Cms.Core;
+using Umbraco.Extensions;
+
+namespace Umbraco.Cms.Api.Common.DependencyInjection;
+
+public class ProcessRequestContextHandler
+    : IOpenIddictServerHandler<OpenIddictServerEvents.ProcessRequestContext>, IOpenIddictValidationHandler<OpenIddictValidationEvents.ProcessRequestContext>
+{
+    private readonly IHttpContextAccessor _httpContextAccessor;
+    private readonly string _backOfficePathSegment;
+
+    public ProcessRequestContextHandler(IHttpContextAccessor httpContextAccessor)
+    {
+        _httpContextAccessor = httpContextAccessor;
+        _backOfficePathSegment = Constants.System.DefaultUmbracoPath.TrimStart(Constants.CharArrays.Tilde)
+            .EnsureStartsWith('/')
+            .EnsureEndsWith('/');
+    }
+
+    public ValueTask HandleAsync(OpenIddictServerEvents.ProcessRequestContext context)
+    {
+        if (SkipOpenIddictHandlingForRequest())
+        {
+            context.SkipRequest();
+        }
+
+        return ValueTask.CompletedTask;
+    }
+
+    public ValueTask HandleAsync(OpenIddictValidationEvents.ProcessRequestContext context)
+    {
+        if (SkipOpenIddictHandlingForRequest())
+        {
+            context.SkipRequest();
+        }
+
+        return ValueTask.CompletedTask;
+    }
+
+    private bool SkipOpenIddictHandlingForRequest()
+    {
+        var requestPath = _httpContextAccessor.HttpContext?.Request.Path.Value;
+        if (requestPath.IsNullOrWhiteSpace())
+        {
+            return false;
+        }
+
+        return requestPath.StartsWith(_backOfficePathSegment) is false;
+    }
+}
diff --git a/src/Umbraco.Cms.Api.Common/DependencyInjection/UmbracoBuilderAuthExtensions.cs b/src/Umbraco.Cms.Api.Common/DependencyInjection/UmbracoBuilderAuthExtensions.cs
index b61f842b5a..7e730695f3 100644
--- a/src/Umbraco.Cms.Api.Common/DependencyInjection/UmbracoBuilderAuthExtensions.cs
+++ b/src/Umbraco.Cms.Api.Common/DependencyInjection/UmbracoBuilderAuthExtensions.cs
@@ -2,6 +2,8 @@ using System.Security.Cryptography;
 using Microsoft.Extensions.Configuration;
 using Microsoft.Extensions.DependencyInjection;
 using Microsoft.IdentityModel.Tokens;
+using OpenIddict.Server;
+using OpenIddict.Validation;
 using Umbraco.Cms.Api.Common.Security;
 using Umbraco.Cms.Core;
 using Umbraco.Cms.Core.Configuration.Models;
@@ -96,6 +98,13 @@ public static class UmbracoBuilderAuthExtensions
                 options
                     .AddEncryptionKey(new SymmetricSecurityKey(RandomNumberGenerator.GetBytes(32))) // generate a cryptographically secure random 256-bits key
                     .AddSigningKey(new RsaSecurityKey(RSA.Create(keySizeInBits: 2048))); // generate RSA key with recommended size of 2048-bits
+
+                // Add custom handler for the "ProcessRequestContext" server event, to stop OpenIddict from handling
+                // every last request to the server (including front-end requests).
+                options.AddEventHandler<OpenIddictServerEvents.ProcessRequestContext>(configuration =>
+                {
+                    configuration.UseSingletonHandler<ProcessRequestContextHandler>().SetOrder(OpenIddict.Server.AspNetCore.OpenIddictServerAspNetCoreHandlers.ResolveRequestUri.Descriptor.Order - 1);
+                });
             })
 
             // Register the OpenIddict validation components.
@@ -113,6 +122,13 @@ public static class UmbracoBuilderAuthExtensions
 
                 // Use ASP.NET Core Data Protection for tokens instead of JWT. (see note in AddServer)
                 options.UseDataProtection();
+
+                // Add custom handler for the "ProcessRequestContext" validation event, to stop OpenIddict from handling
+                // every last request to the server (including front-end requests).
+                options.AddEventHandler<OpenIddictValidationEvents.ProcessRequestContext>(configuration =>
+                {
+                    configuration.UseSingletonHandler<ProcessRequestContextHandler>().SetOrder(OpenIddict.Validation.AspNetCore.OpenIddictValidationAspNetCoreHandlers.ResolveRequestUri.Descriptor.Order - 1);
+                });
             });
 
         builder.Services.AddRecurringBackgroundJob<OpenIddictCleanupJob>();