diff --git a/src/Aspire.Hosting.GitHub.Models/GitHubModelResource.cs b/src/Aspire.Hosting.GitHub.Models/GitHubModelResource.cs
index a6c441e38ac..054e8f8ce0c 100644
--- a/src/Aspire.Hosting.GitHub.Models/GitHubModelResource.cs
+++ b/src/Aspire.Hosting.GitHub.Models/GitHubModelResource.cs
@@ -10,6 +10,8 @@ namespace Aspire.Hosting.GitHub.Models;
 /// </summary>
 public class GitHubModelResource : Resource, IResourceWithConnectionString, IResourceWithoutLifetime
 {
+    internal ParameterResource DefaultKeyParameter { get; set; }
+
     /// <summary>
     /// Initializes a new instance of the <see cref="GitHubModelResource"/> class.
     /// </summary>
@@ -21,7 +23,7 @@ public GitHubModelResource(string name, string model, ParameterResource? organiz
     {
         Model = model;
         Organization = organization;
-        Key = key;
+        Key = DefaultKeyParameter = key;
     }
 
     /// <summary>
diff --git a/src/Aspire.Hosting.GitHub.Models/GitHubModelsExtensions.cs b/src/Aspire.Hosting.GitHub.Models/GitHubModelsExtensions.cs
index 7b68c6ac2d2..34ca285214d 100644
--- a/src/Aspire.Hosting.GitHub.Models/GitHubModelsExtensions.cs
+++ b/src/Aspire.Hosting.GitHub.Models/GitHubModelsExtensions.cs
@@ -85,8 +85,11 @@ public static IResourceBuilder<GitHubModelResource> WithApiKey(this IResourceBui
             throw new ArgumentException("The API key parameter must be marked as secret. Use AddParameter with secret: true when creating the parameter.", nameof(apiKey));
         }
 
-        // Remove the existing API key parameter
-        builder.ApplicationBuilder.Resources.Remove(builder.Resource.Key);
+        // Remove the existing parameter if it's the default one
+        if (builder.Resource.DefaultKeyParameter == builder.Resource.Key)
+        {
+            builder.ApplicationBuilder.Resources.Remove(builder.Resource.Key);
+        }
 
         builder.Resource.Key = apiKey.Resource;
 
diff --git a/tests/Aspire.Hosting.GitHub.Models.Tests/GitHubModelsExtensionTests.cs b/tests/Aspire.Hosting.GitHub.Models.Tests/GitHubModelsExtensionTests.cs
index 0ea7e0e2951..89dd0499ba3 100644
--- a/tests/Aspire.Hosting.GitHub.Models.Tests/GitHubModelsExtensionTests.cs
+++ b/tests/Aspire.Hosting.GitHub.Models.Tests/GitHubModelsExtensionTests.cs
@@ -254,6 +254,26 @@ public void WithApiKeySucceedsIfParameterIsSecret()
         Assert.Equal(apiKey.Resource, github.Resource.Key);
     }
 
+    [Fact]
+    public void WithApiKeyCalledTwiceOnlyRemovesDefaultParameter()
+    {
+        using var builder = TestDistributedApplicationBuilder.Create();
+
+        var github = builder.AddGitHubModel("github", "openai/gpt-4o-mini");
+
+        Assert.NotNull(builder.Resources.FirstOrDefault(r => r.Name == "github-gh-apikey"));
+
+        github.WithApiKey(builder.AddParameter("secret-key1", secret: true));
+
+        Assert.Null(builder.Resources.FirstOrDefault(r => r.Name == "github-gh-apikey"));
+        Assert.NotNull(builder.Resources.FirstOrDefault(r => r.Name == "secret-key1"));
+
+        github.WithApiKey(builder.AddParameter("secret-key2", secret: true));
+
+        Assert.NotNull(builder.Resources.FirstOrDefault(r => r.Name == "secret-key1"));
+        Assert.NotNull(builder.Resources.FirstOrDefault(r => r.Name == "secret-key2"));
+    }
+
     [Fact]
     public void WithHealthCheckAddsHealthCheckAnnotation()
     {