diff --git a/src/Aspire.Hosting.NodeJs/NodeExtensions.cs b/src/Aspire.Hosting.NodeJs/NodeExtensions.cs
index 4f4c8169724..4bdd94818c8 100644
--- a/src/Aspire.Hosting.NodeJs/NodeExtensions.cs
+++ b/src/Aspire.Hosting.NodeJs/NodeExtensions.cs
@@ -74,13 +74,14 @@ private static IResourceBuilder<NodeAppResource> WithNodeDefaults(this IResource
             .WithEnvironment("NODE_ENV", builder.ApplicationBuilder.Environment.IsDevelopment() ? "development" : "production")
             .WithExecutableCertificateTrustCallback((ctx) =>
             {
-                if (ctx.Scope == CustomCertificateAuthoritiesScope.Append)
+                if (ctx.Scope == CertificateTrustScope.Append)
                 {
                     ctx.CertificateBundleEnvironment.Add("NODE_EXTRA_CA_CERTS");
                 }
                 else
                 {
                     ctx.CertificateTrustArguments.Add("--use-openssl-ca");
+                    ctx.CertificateBundleEnvironment.Add("SSL_CERT_FILE");
                 }
 
                 return Task.CompletedTask;
diff --git a/src/Aspire.Hosting.Python/PythonAppResourceBuilderExtensions.cs b/src/Aspire.Hosting.Python/PythonAppResourceBuilderExtensions.cs
index c5522fae7ba..55a87f74f6b 100644
--- a/src/Aspire.Hosting.Python/PythonAppResourceBuilderExtensions.cs
+++ b/src/Aspire.Hosting.Python/PythonAppResourceBuilderExtensions.cs
@@ -3,6 +3,7 @@
 
 using System.ComponentModel;
 using System.Runtime.CompilerServices;
+
 #pragma warning disable ASPIREEXTENSION001
 using Aspire.Hosting.ApplicationModel;
 using Aspire.Hosting.Python;
@@ -281,20 +282,30 @@ private static IResourceBuilder<PythonAppResource> AddPythonAppCore(
         });
 
         // Configure required environment variables for custom certificate trust when running as an executable
-        resourceBuilder.WithExecutableCertificateTrustCallback(ctx =>
-        {
-            if (ctx.Scope == CustomCertificateAuthoritiesScope.Override)
+        // Python defaults to using System scope to allow combining custom CAs with system CAs as there's no clean
+        // way to simply append additional certificates to default Python trust stores such as certifi.
+        resourceBuilder
+            .WithCertificateTrustScope(CertificateTrustScope.System)
+            .WithExecutableCertificateTrustCallback(ctx =>
             {
-                // See: https://docs.python-requests.org/en/latest/user/advanced/#ssl-cert-verification
-                ctx.CertificateBundleEnvironment.Add("REQUESTS_CA_BUNDLE");
-            }
+                if (ctx.Scope != CertificateTrustScope.Append)
+                {
+                    // Override default certificates path for the requests module.
+                    // See: https://docs.python-requests.org/en/latest/user/advanced/#ssl-cert-verification
+                    ctx.CertificateBundleEnvironment.Add("REQUESTS_CA_BUNDLE");
+
+                    // Override default certificates path for Python modules that honor OpenSSL style paths.
+                    // This has been tested with urllib, urllib3, httpx, and aiohttp.
+                    // See: https://docs.openssl.org/3.0/man3/SSL_CTX_load_verify_locations/#description
+                    ctx.CertificateBundleEnvironment.Add("SSL_CERT_FILE");
+                }
 
-            // Override default opentelemetry-python certificate bundle path
-            // See: https://opentelemetry-python.readthedocs.io/en/latest/exporter/otlp/otlp.html#module-opentelemetry.exporter.otlp
-            ctx.CertificateBundleEnvironment.Add("OTEL_EXPORTER_OTLP_CERTIFICATE");
+                // Override default opentelemetry-python certificate bundle path
+                // See: https://opentelemetry-python.readthedocs.io/en/latest/exporter/otlp/otlp.html#module-opentelemetry.exporter.otlp
+                ctx.CertificateBundleEnvironment.Add("OTEL_EXPORTER_OTLP_CERTIFICATE");
 
-            return Task.CompletedTask;
-        });
+                return Task.CompletedTask;
+            });
 
         // VS Code debug support - only applicable for Script and Module types
         if (entrypointType is EntrypointType.Script or EntrypointType.Module)
diff --git a/src/Aspire.Hosting/ApplicationModel/CertificateAuthorityCollectionAnnotation.cs b/src/Aspire.Hosting/ApplicationModel/CertificateAuthorityCollectionAnnotation.cs
index 8b67ce5203e..0d4deb0006e 100644
--- a/src/Aspire.Hosting/ApplicationModel/CertificateAuthorityCollectionAnnotation.cs
+++ b/src/Aspire.Hosting/ApplicationModel/CertificateAuthorityCollectionAnnotation.cs
@@ -4,18 +4,32 @@
 namespace Aspire.Hosting.ApplicationModel;
 
 /// <summary>
-/// Defines the scope of custom certificate authorities for a resource. The default is <see cref="Append"/>.
+/// Defines the scope of custom certificate authorities for a resource. The default scope for most resources
+/// is <see cref="Append"/>, but some resources may choose to override this default behavior.
 /// </summary>
-public enum CustomCertificateAuthoritiesScope
+public enum CertificateTrustScope
 {
     /// <summary>
-    /// Append the specified certificate authorities to the default set of trusted CAs for a resource.
+    /// Append the specified certificate authorities to the default set of trusted CAs for a resource. Not all
+    /// resources support this mode, in which case custom certificate authorities may not be applied. In that case,
+    /// consider using <see cref="Override"/> or <see cref="System"/> instead.
     /// </summary>
     Append,
     /// <summary>
     /// Replace the default set of trusted CAs for a resource with the specified certificate authorities.
     /// </summary>
     Override,
+    /// <summary>
+    /// Attempt to configure the resource to trust the default system certificate authorities in addition to
+    /// any configured custom certificate trust. This mode is useful for resources that don't otherwise
+    /// allow appending to their default trusted certificate authorities but do allow overriding the set
+    /// of trusted certificates (e.g. Python, Rust, etc.).
+    /// </summary>
+    System,
+    /// <summary>
+    /// Disable all custom certificate authority configuration for a resource.
+    /// </summary>
+    None,
 }
 
 /// <summary>
@@ -37,5 +51,5 @@ public sealed class CertificateAuthorityCollectionAnnotation : IResourceAnnotati
     /// Gets a value indicating whether the resource should attempt to override its default CA trust behavior in
     /// favor of the provided certificates (not all resources will support this).
     /// </summary>
-    public CustomCertificateAuthoritiesScope? Scope { get; internal set; }
+    public CertificateTrustScope? Scope { get; internal set; }
 }
diff --git a/src/Aspire.Hosting/ApplicationModel/ContainerCertificateTrustCallbackAnnotation.cs b/src/Aspire.Hosting/ApplicationModel/ContainerCertificateTrustCallbackAnnotation.cs
index 602f514143a..4d051e9b3de 100644
--- a/src/Aspire.Hosting/ApplicationModel/ContainerCertificateTrustCallbackAnnotation.cs
+++ b/src/Aspire.Hosting/ApplicationModel/ContainerCertificateTrustCallbackAnnotation.cs
@@ -28,9 +28,9 @@ public sealed class ContainerCertificateTrustCallbackAnnotationContext
     public required IResource Resource { get; init; }
 
     /// <summary>
-    /// Gets the <see cref="CustomCertificateAuthoritiesScope"/> of trust for the resource.
+    /// Gets the <see cref="CertificateTrustScope"/> of trust for the resource.
     /// </summary>
-    public required CustomCertificateAuthoritiesScope Scope { get; init; }
+    public required CertificateTrustScope Scope { get; init; }
 
     /// <summary>
     /// Gets the <see cref="X509Certificate2Collection"/> of certificates for this resource.
@@ -72,7 +72,7 @@ public sealed class ContainerCertificateTrustCallbackAnnotationContext
 
     /// <summary>
     /// List of default certificate bundle files in the container that will be replaced if the resource scope of trust is
-    /// set to <see cref="CustomCertificateAuthoritiesScope.Override"/>. Defaults to common Linux paths for CA certificates
+    /// set to <see cref="CertificateTrustScope.Override"/>. Defaults to common Linux paths for CA certificates
     /// to maximize compatibility, but can be overriden with specific paths for a given resource if needed.
     /// See: https://go.dev/src/crypto/x509/root_linux.go
     /// </summary>
@@ -94,7 +94,7 @@ public sealed class ContainerCertificateTrustCallbackAnnotationContext
 
     /// <summary>
     /// List of default certificate directories in a container that should be appended to the custom certificate directories in
-    /// <see cref="CustomCertificateAuthoritiesScope.Append"/> mode. Defaults to common Linux paths for CA certificates.
+    /// <see cref="CertificateTrustScope.Append"/> mode. Defaults to common Linux paths for CA certificates.
     /// See: https://go.dev/src/crypto/x509/root_linux.go
     /// </summary>
     public List<string> DefaultContainerCertificatesDirectoryPaths { get; } = new()
diff --git a/src/Aspire.Hosting/ApplicationModel/ExecutableCertificateTrustCallbackAnnotation.cs b/src/Aspire.Hosting/ApplicationModel/ExecutableCertificateTrustCallbackAnnotation.cs
index 0fee2619763..fd4d87a2475 100644
--- a/src/Aspire.Hosting/ApplicationModel/ExecutableCertificateTrustCallbackAnnotation.cs
+++ b/src/Aspire.Hosting/ApplicationModel/ExecutableCertificateTrustCallbackAnnotation.cs
@@ -28,9 +28,9 @@ public sealed class ExecutableCertificateTrustCallbackAnnotationContext
     public required IResource Resource { get; init; }
 
     /// <summary>
-    /// Gets the <see cref="CustomCertificateAuthoritiesScope"/> of trust for the resource.
+    /// Gets the <see cref="CertificateTrustScope"/> of trust for the resource.
     /// </summary>
-    public required CustomCertificateAuthoritiesScope Scope { get; init; }
+    public required CertificateTrustScope Scope { get; init; }
 
     /// <summary>
     /// Gets the <see cref="X509Certificate2Collection"/> of certificates for this resource.
diff --git a/src/Aspire.Hosting/Dcp/DcpExecutor.cs b/src/Aspire.Hosting/Dcp/DcpExecutor.cs
index 54326438ecc..acb56f39474 100644
--- a/src/Aspire.Hosting/Dcp/DcpExecutor.cs
+++ b/src/Aspire.Hosting/Dcp/DcpExecutor.cs
@@ -2055,7 +2055,7 @@ await modelResource.ProcessContainerRuntimeArgValues(
         bool trustDevCert = _distributedApplicationOptions.TrustDeveloperCertificate;
 
         var certificates = new X509Certificate2Collection();
-        var scope = CustomCertificateAuthoritiesScope.Append;
+        var scope = CertificateTrustScope.Append;
         if (modelResource.TryGetLastAnnotation<CertificateAuthorityCollectionAnnotation>(out var caAnnotation))
         {
             foreach (var certCollection in caAnnotation.CertificateAuthorityCollections)
@@ -2067,6 +2067,17 @@ await modelResource.ProcessContainerRuntimeArgValues(
             scope = caAnnotation.Scope.GetValueOrDefault(scope);
         }
 
+        if (scope == CertificateTrustScope.None)
+        {
+            return (new List<string>(), new List<EnvVar>(), false);
+        }
+
+        if (scope == CertificateTrustScope.System)
+        {
+            // Read the system root certificates and add them to the collection
+            certificates.AddRootCertificates();
+        }
+
         if (trustDevCert)
         {
             foreach (var cert in _developerCertificateService.Certificates)
@@ -2164,7 +2175,7 @@ await modelResource.ProcessContainerRuntimeArgValues(
         bool trustDevCert = _distributedApplicationOptions.TrustDeveloperCertificate;
 
         var certificates = new X509Certificate2Collection();
-        var scope = CustomCertificateAuthoritiesScope.Append;
+        var scope = CertificateTrustScope.Append;
         if (modelResource.TryGetLastAnnotation<CertificateAuthorityCollectionAnnotation>(out var caAnnotation))
         {
             foreach (var certCollection in caAnnotation.CertificateAuthorityCollections)
@@ -2176,6 +2187,18 @@ await modelResource.ProcessContainerRuntimeArgValues(
             scope = caAnnotation.Scope.GetValueOrDefault(scope);
         }
 
+        if (scope == CertificateTrustScope.None)
+        {
+            // Resource has disabled custom certificate authorities
+            return (new List<string>(), new List<EnvVar>(), new List<ContainerCreateFileSystem>(), false);
+        }
+
+        if (scope == CertificateTrustScope.System)
+        {
+            // Read the system root certificates and add them to the collection
+            certificates.AddRootCertificates();
+        }
+
         if (trustDevCert)
         {
             foreach (var cert in _developerCertificateService.Certificates)
@@ -2191,10 +2214,11 @@ await modelResource.ProcessContainerRuntimeArgValues(
             Certificates = certificates,
             CancellationToken = cancellationToken
         };
-        if (scope == CustomCertificateAuthoritiesScope.Override)
+
+        if (scope != CertificateTrustScope.Append)
         {
-            // Override default OpenSSL certificate bundle path resolution
-            // SSL_CERT_FILE is always added to the defaults when the scope is Override
+            // When Override or System scope is set (not Append), override the default OpenSSL certificate bundle path
+            // resolution by setting the SSL_CERT_FILE environment variable.
             // See: https://docs.openssl.org/3.0/man3/SSL_CTX_load_verify_locations/#description
             context.CertificateBundleEnvironment.Add("SSL_CERT_FILE");
         }
@@ -2254,7 +2278,7 @@ await modelResource.ProcessContainerRuntimeArgValues(
             }
 
             var caDirEnvValue = caFilesPath;
-            if (scope == CustomCertificateAuthoritiesScope.Append)
+            if (scope == CertificateTrustScope.Append)
             {
                 foreach (var defaultCaDir in context.DefaultContainerCertificatesDirectoryPaths)
                 {
@@ -2313,9 +2337,9 @@ await modelResource.ProcessContainerRuntimeArgValues(
                 ],
             });
 
-            if (scope == CustomCertificateAuthoritiesScope.Override)
+            if (scope != CertificateTrustScope.Append)
             {
-                // If overriding the system CA bundle, then we want to copy our bundle to the well-known locations
+                // If overriding the default resource CA bundle, then we want to copy our bundle to the well-known locations
                 // used by common Linux distributions to make it easier to ensure applications pick it up.
                 foreach (var bundlePath in context.DefaultContainerCertificateAuthorityBundlePaths)
                 {
diff --git a/src/Aspire.Hosting/ResourceBuilderExtensions.cs b/src/Aspire.Hosting/ResourceBuilderExtensions.cs
index 62be4407397..188c016a5c7 100644
--- a/src/Aspire.Hosting/ResourceBuilderExtensions.cs
+++ b/src/Aspire.Hosting/ResourceBuilderExtensions.cs
@@ -2156,16 +2156,16 @@ public static IResourceBuilder<TResource> WithDeveloperCertificateTrust<TResourc
     }
 
     /// <summary>
-    /// Sets the <see cref="CustomCertificateAuthoritiesScope"/> for custom certificate authorities associated with the resource.
+    /// Sets the <see cref="CertificateTrustScope"/> for custom certificate authorities associated with the resource.
     /// </summary>
     /// <typeparam name="TResource">The type of the resource.</typeparam>
     /// <param name="builder">The resource builder.</param>
     /// <param name="scope">The scope to apply to custom certificate authorities associated with the resource.</param>
     /// <returns>The <see cref="IResourceBuilder{TResource}"/>.</returns>
     /// <remarks>
-    /// The default scope is <see cref="CustomCertificateAuthoritiesScope.Append"/> which means that custom certificate authorities
-    /// should be appended to the default trusted certificate authorities for the resource. Setting the scope to
-    /// <see cref="CustomCertificateAuthoritiesScope.Override"/> indicates the set of certificates in referenced
+    /// The default scope if not overridden is <see cref="CertificateTrustScope.Append"/> which means that custom certificate
+    /// authorities should be appended to the default trusted certificate authorities for the resource. Setting the scope to
+    /// <see cref="CertificateTrustScope.Override"/> indicates the set of certificates in referenced
     /// <see cref="CertificateAuthorityCollection"/> (and optionally Aspire developer certificiates) should be used as the
     /// exclusive source of trust for a resource.
     /// In all cases, this is a best effort implementation as not all resources support full customization of certificate
@@ -2178,11 +2178,11 @@ public static IResourceBuilder<TResource> WithDeveloperCertificateTrust<TResourc
     ///
     /// var container = builder.AddContainer("my-service", "my-service:latest")
     ///     .WithCertificateAuthorityCollection(caCollection)
-    ///     .WithCustomCertificateAuthoritiesScope(CustomCertificateAuthoritiesScope.Override);
+    ///     .WithCertificateTrustScope(CertificateTrustScope.Override);
     /// </code>
     /// </example>
     /// </remarks>
-    public static IResourceBuilder<TResource> WithCustomCertificateAuthoritiesScope<TResource>(this IResourceBuilder<TResource> builder, CustomCertificateAuthoritiesScope scope)
+    public static IResourceBuilder<TResource> WithCertificateTrustScope<TResource>(this IResourceBuilder<TResource> builder, CertificateTrustScope scope)
         where TResource : IResourceWithEnvironment, IResourceWithArgs
     {
         ArgumentNullException.ThrowIfNull(builder);
diff --git a/src/Aspire.Hosting/Utils/X509Certificate2Extensions.cs b/src/Aspire.Hosting/Utils/X509Certificate2Extensions.cs
index 7781b0e3c11..1531556bf99 100644
--- a/src/Aspire.Hosting/Utils/X509Certificate2Extensions.cs
+++ b/src/Aspire.Hosting/Utils/X509Certificate2Extensions.cs
@@ -78,4 +78,26 @@ public static bool SupportsContainerTrust(this X509Certificate2 certificate)
 
         return true;
     }
+
+    /// <summary>
+    /// Adds certificates from the system root stores to the specified collection.
+    /// </summary>
+    /// <param name="collection">The <see cref="X509Certificate2Collection"/> to add the certificates to.</param>
+    public static void AddRootCertificates(this X509Certificate2Collection collection)
+    {
+        ArgumentNullException.ThrowIfNull(collection);
+
+        var locations = new[]
+        {
+            (StoreName.Root, StoreLocation.CurrentUser),
+            (StoreName.Root, StoreLocation.LocalMachine),
+        };
+
+        foreach (var (storeName, storeLocation) in locations)
+        {
+            using var store = new X509Store(storeName, storeLocation);
+            store.Open(OpenFlags.ReadOnly);
+            collection.AddRange(store.Certificates);
+        }
+    }
 }
\ No newline at end of file