diff --git a/src/Aspire.Hosting/ProjectResourceBuilderExtensions.cs b/src/Aspire.Hosting/ProjectResourceBuilderExtensions.cs
index 5f601062be4..35408653002 100644
--- a/src/Aspire.Hosting/ProjectResourceBuilderExtensions.cs
+++ b/src/Aspire.Hosting/ProjectResourceBuilderExtensions.cs
@@ -402,11 +402,27 @@ private static IResourceBuilder<ProjectResource> WithProjectDefaults(this IResou
             if (!kestrelEndpointsByScheme.Any())
             {
                 var urlsFromApplicationUrl = launchProfile.ApplicationUrl?.Split(';', StringSplitOptions.RemoveEmptyEntries) ?? [];
+                Dictionary<string, int> endpointCountByScheme = [];
                 foreach (var url in urlsFromApplicationUrl)
                 {
                     var uri = new Uri(url);
 
-                    builder.WithEndpoint(uri.Scheme, e =>
+                    // Keep track of how many endpoints we have for each scheme
+                    endpointCountByScheme.TryGetValue(uri.Scheme, out var count);
+                    endpointCountByScheme[uri.Scheme] = count + 1;
+
+                    // If we have multiple for the same scheme, we differentiate them by appending a number.
+                    // We only do this starting with the second endpoint, so that the first stays just http/https.
+                    // This allows us to keep the same behavior as "dotnet run".
+                    // Also, note that we only do this in Run mode, as in Publish mode those extra endpoints
+                    // with generic names would not be easily usable.
+                    var endpointName = uri.Scheme;
+                    if (endpointCountByScheme[uri.Scheme] > 1)
+                    {
+                        endpointName += endpointCountByScheme[uri.Scheme];
+                    }
+
+                    builder.WithEndpoint(endpointName, e =>
                     {
                         e.Port = uri.Port;
                         e.UriScheme = uri.Scheme;
diff --git a/tests/Aspire.Hosting.Tests/ProjectResourceTests.cs b/tests/Aspire.Hosting.Tests/ProjectResourceTests.cs
index f7d3532c604..a0395440134 100644
--- a/tests/Aspire.Hosting.Tests/ProjectResourceTests.cs
+++ b/tests/Aspire.Hosting.Tests/ProjectResourceTests.cs
@@ -410,6 +410,35 @@ public async Task ProjectWithLaunchProfileAddsHttpOrHttpsEndpointAddsToEnv()
         Assert.False(config.ContainsKey("ASPNETCORE_HTTPS_PORT"));
     }
 
+    [Fact]
+    public async Task ProjectWithMultipleLaunchProfileAppUrlsGetsAllUrls()
+    {
+        var appBuilder = CreateBuilder(operation: DistributedApplicationOperation.Run);
+
+        var builder = appBuilder.AddProject<TestProjectWithManyAppUrlsInLaunchSettings>("projectName");
+
+        // Need to allocated all the endpoints we get from the launch profile applicationUrl
+        var index = 0;
+        foreach (var q in new[] { "http", "http2", "https", "https2", "https3" })
+        {
+            builder.WithEndpoint(q, e =>
+            {
+                e.AllocatedEndpoint = new(e, "localhost", e.Port!.Value, targetPortExpression: $"p{index++}");
+            });
+        }
+
+        using var app = appBuilder.Build();
+        var appModel = app.Services.GetRequiredService<DistributedApplicationModel>();
+        var projectResources = appModel.GetProjectResources();
+        var resource = Assert.Single(projectResources);
+        var config = await EnvironmentVariableEvaluator.GetEnvironmentVariablesAsync(resource, DistributedApplicationOperation.Run, TestServiceProvider.Instance);
+
+        Assert.Equal("https://localhost:p2;http://localhost:p0;http://localhost:p1;https://localhost:p3;https://localhost:p4", config["ASPNETCORE_URLS"]);
+
+        // The first https port is the one that should be used for ASPNETCORE_HTTPS_PORT
+        Assert.Equal("7144", config["ASPNETCORE_HTTPS_PORT"]);
+    }
+
     [Fact]
     public void DisabledForwardedHeadersAddsAnnotationToProject()
     {
@@ -618,4 +647,25 @@ public TestProjectWithLaunchSettings()
             };
         }
     }
+
+    private sealed class TestProjectWithManyAppUrlsInLaunchSettings : BaseProjectWithProfileAndConfig
+    {
+        public TestProjectWithManyAppUrlsInLaunchSettings()
+        {
+            Profiles = new()
+            {
+                ["https"] = new()
+                {
+                    CommandName = "Project",
+                    CommandLineArgs = "arg1 arg2",
+                    LaunchBrowser = true,
+                    ApplicationUrl = "https://localhost:7144;http://localhost:5193;http://localhost:5194;https://localhost:7145;https://localhost:7146",
+                    EnvironmentVariables = new()
+                    {
+                        ["ASPNETCORE_ENVIRONMENT"] = "Development"
+                    }
+                }
+            };
+        }
+    }
 }