diff --git a/docs/specs/dashboard-http-api.md b/docs/specs/dashboard-http-api.md
index e1daf534b38..4b6e62c8882 100644
--- a/docs/specs/dashboard-http-api.md
+++ b/docs/specs/dashboard-http-api.md
@@ -49,7 +49,7 @@ The API can be enabled/disabled and configured via `Dashboard:Api` settings:
 
 | Setting | Values | Default | Description |
 |---------|--------|---------|-------------|
-| `Enabled` | `true`, `false` | `true` | Whether the Telemetry HTTP API is enabled |
+| `Enabled` | `true`, `false` | `true` when frontend is unsecured or an API key is configured; `false` when the frontend requires authentication and no API key is set | Whether the Telemetry HTTP API is enabled |
 | `AuthMode` | `ApiKey`, `Unsecured` | `Unsecured` | Authentication mode for the API |
 | `PrimaryApiKey` | string | - | API key for authentication (required when `AuthMode=ApiKey`) |
 | `SecondaryApiKey` | string | - | Optional secondary API key for key rotation |
@@ -58,6 +58,7 @@ The API can be enabled/disabled and configured via `Dashboard:Api` settings:
 
 - The API shares the same port as the Dashboard frontend (default: 18888).
 - Hosters may set `Enabled: false` to disable the API for security.
+- When the frontend requires authentication (e.g., OpenID Connect) and no API key is configured, the API is disabled by default. Set `Enabled: true` explicitly to override.
 - API keys are shared with MCP configuration—setting either configures both.
 - When running in unsecured mode, a warning is logged on first API request.
 
diff --git a/src/Aspire.Dashboard/Configuration/DashboardOptions.cs b/src/Aspire.Dashboard/Configuration/DashboardOptions.cs
index 7a14a80af5e..d76daf200a8 100644
--- a/src/Aspire.Dashboard/Configuration/DashboardOptions.cs
+++ b/src/Aspire.Dashboard/Configuration/DashboardOptions.cs
@@ -149,8 +149,10 @@ public sealed class ApiOptions
 
     /// <summary>
     /// Gets or sets whether the Telemetry HTTP API is enabled.
-    /// When false, the /api/telemetry/* endpoints are not registered.
-    /// Defaults to true.
+    /// When <see langword="false"/>, the /api/telemetry/* endpoints are not registered.
+    /// Defaults to <see langword="true"/> when the dashboard frontend is unsecured or an API key is configured.
+    /// Defaults to <see langword="false"/> when the frontend requires authentication (e.g., OpenID Connect
+    /// or BrowserToken) and no API key is configured, to prevent unauthenticated access to telemetry data.
     /// </summary>
     public bool? Enabled { get; set; }
 
diff --git a/src/Aspire.Dashboard/Configuration/PostConfigureDashboardOptions.cs b/src/Aspire.Dashboard/Configuration/PostConfigureDashboardOptions.cs
index b166dfda5b4..717a400c119 100644
--- a/src/Aspire.Dashboard/Configuration/PostConfigureDashboardOptions.cs
+++ b/src/Aspire.Dashboard/Configuration/PostConfigureDashboardOptions.cs
@@ -73,6 +73,16 @@ public void PostConfigure(string? name, DashboardOptions options)
             // If an API key is configured, default to ApiKey auth mode instead of Unsecured.
             options.Mcp.AuthMode ??= string.IsNullOrEmpty(options.Mcp.PrimaryApiKey) ? McpAuthMode.Unsecured : McpAuthMode.ApiKey;
             options.Api.AuthMode ??= string.IsNullOrEmpty(options.Api.PrimaryApiKey) ? ApiAuthMode.Unsecured : ApiAuthMode.ApiKey;
+
+            // When the frontend requires authentication (e.g. OpenID Connect or BrowserToken) but the API
+            // has no key configured (and would therefore default to Unsecured), disable the API by default
+            // to prevent unauthenticated access to telemetry data on the same port.
+            if (options.Api.Enabled is null &&
+                options.Frontend.AuthMode is not FrontendAuthMode.Unsecured &&
+                options.Api.AuthMode is ApiAuthMode.Unsecured)
+            {
+                options.Api.Enabled = false;
+            }
         }
 
         if (options.Frontend.AuthMode == FrontendAuthMode.BrowserToken && string.IsNullOrEmpty(options.Frontend.BrowserToken))
diff --git a/tests/Aspire.Dashboard.Tests/Integration/TelemetryApiTests.cs b/tests/Aspire.Dashboard.Tests/Integration/TelemetryApiTests.cs
index 822559e11ff..05f67c3801c 100644
--- a/tests/Aspire.Dashboard.Tests/Integration/TelemetryApiTests.cs
+++ b/tests/Aspire.Dashboard.Tests/Integration/TelemetryApiTests.cs
@@ -82,6 +82,86 @@ public async Task Configuration_ApiKeyExplicit_OverridesMcp()
         Assert.Equal(apiKey.Length, options.Api.GetPrimaryApiKeyBytesOrNull()!.Length);
     }
 
+    [Fact]
+    public async Task Configuration_ApiDefaultsToDisabled_WhenFrontendIsBrowserToken()
+    {
+        // Arrange - BrowserToken frontend with no API key configured
+        await using var app = IntegrationTestHelpers.CreateDashboardWebApplication(_testOutputHelper, config =>
+        {
+            config[DashboardConfigNames.DashboardFrontendAuthModeName.ConfigKey] = FrontendAuthMode.BrowserToken.ToString();
+            // Don't set any Api config — no API key
+        });
+        await app.StartAsync().DefaultTimeout();
+
+        // Assert - API should default to disabled when frontend has auth but no API key
+        var options = app.Services.GetRequiredService<IOptionsMonitor<DashboardOptions>>().CurrentValue;
+        Assert.False(options.Api.Enabled);
+    }
+
+    [Fact]
+    public async Task Configuration_ApiStaysEnabled_WhenExplicitlyEnabled()
+    {
+        // Arrange - BrowserToken frontend, explicitly enable API with API key auth
+        var apiKey = "TestKey123!";
+        await using var app = IntegrationTestHelpers.CreateDashboardWebApplication(_testOutputHelper, config =>
+        {
+            config[DashboardConfigNames.DashboardFrontendAuthModeName.ConfigKey] = FrontendAuthMode.BrowserToken.ToString();
+            config[DashboardConfigNames.DashboardApiEnabledName.ConfigKey] = "true";
+            config[DashboardConfigNames.DashboardApiAuthModeName.ConfigKey] = ApiAuthMode.ApiKey.ToString();
+            config[DashboardConfigNames.DashboardApiPrimaryApiKeyName.ConfigKey] = apiKey;
+        });
+        await app.StartAsync().DefaultTimeout();
+
+        // Assert - API should be enabled because explicitly configured
+        var options = app.Services.GetRequiredService<IOptionsMonitor<DashboardOptions>>().CurrentValue;
+        Assert.True(options.Api.Enabled);
+
+        using var httpClient = IntegrationTestHelpers.CreateHttpClient($"http://{app.FrontendSingleEndPointAccessor().EndPoint}");
+        httpClient.DefaultRequestHeaders.TryAddWithoutValidation(ApiAuthenticationHandler.ApiKeyHeaderName, apiKey);
+        var response = await httpClient.GetAsync("/api/telemetry/spans").DefaultTimeout();
+        Assert.Equal(HttpStatusCode.OK, response.StatusCode);
+    }
+
+    [Fact]
+    public async Task Configuration_ApiStaysEnabled_WhenApiKeyConfigured()
+    {
+        // Arrange - BrowserToken frontend with API key configured (should auto-enable ApiKey auth mode)
+        var apiKey = "TestKey123!";
+        await using var app = IntegrationTestHelpers.CreateDashboardWebApplication(_testOutputHelper, config =>
+        {
+            config[DashboardConfigNames.DashboardFrontendAuthModeName.ConfigKey] = FrontendAuthMode.BrowserToken.ToString();
+            config[DashboardConfigNames.DashboardApiPrimaryApiKeyName.ConfigKey] = apiKey;
+        });
+        await app.StartAsync().DefaultTimeout();
+
+        // Assert - API should be enabled because an API key is configured (AuthMode defaults to ApiKey)
+        var options = app.Services.GetRequiredService<IOptionsMonitor<DashboardOptions>>().CurrentValue;
+        Assert.Equal(ApiAuthMode.ApiKey, options.Api.AuthMode);
+        Assert.NotEqual(false, options.Api.Enabled);
+    }
+
+    [Fact]
+    public async Task Configuration_ApiStaysEnabled_WhenFrontendUnsecured()
+    {
+        // Arrange - Unsecured frontend with no API key configured
+        await using var app = IntegrationTestHelpers.CreateDashboardWebApplication(_testOutputHelper, config =>
+        {
+            config[DashboardConfigNames.DashboardFrontendAuthModeName.ConfigKey] = FrontendAuthMode.Unsecured.ToString();
+            // Don't set any Api config
+        });
+        await app.StartAsync().DefaultTimeout();
+
+        // Assert - API should remain enabled when frontend is also unsecured
+        var options = app.Services.GetRequiredService<IOptionsMonitor<DashboardOptions>>().CurrentValue;
+        Assert.NotEqual(false, options.Api.Enabled);
+        Assert.Equal(ApiAuthMode.Unsecured, options.Api.AuthMode);
+
+        // Verify endpoints work
+        using var httpClient = IntegrationTestHelpers.CreateHttpClient($"http://{app.FrontendSingleEndPointAccessor().EndPoint}");
+        var response = await httpClient.GetAsync("/api/telemetry/spans").DefaultTimeout();
+        Assert.Equal(HttpStatusCode.OK, response.StatusCode);
+    }
+
     #endregion
 
     [Fact]