diff --git a/cli/azd/extensions/azure.ai.agents/internal/cmd/invoke.go b/cli/azd/extensions/azure.ai.agents/internal/cmd/invoke.go
index 082020f1e32..0ce052005ca 100644
--- a/cli/azd/extensions/azure.ai.agents/internal/cmd/invoke.go
+++ b/cli/azd/extensions/azure.ai.agents/internal/cmd/invoke.go
@@ -378,9 +378,8 @@ func (a *InvokeAction) responsesLocal(ctx context.Context) error {
 	}
 
 	if resp.StatusCode >= 400 {
-		requestID := resp.Header.Get("apim-request-id")
-		if requestID != "" {
-			fmt.Printf("Trace ID: %s\n", requestID)
+		if traceID := responseTraceID(resp); traceID != "" {
+			fmt.Printf("Trace ID:     %s\n", traceID)
 		}
 		return fmt.Errorf(
 			"POST %s failed with HTTP %d: %s\n%s",
@@ -614,9 +613,8 @@ func (a *InvokeAction) responsesRemote(ctx context.Context) error {
 	}
 	defer resp.Body.Close()
 
-	requestID := resp.Header.Get("apim-request-id")
-	if requestID != "" {
-		fmt.Printf("Trace ID: %s\n", requestID)
+	if traceID := responseTraceID(resp); traceID != "" {
+		fmt.Printf("Trace ID:     %s\n", traceID)
 	}
 
 	captureResponseSession(ctx, rc.azdClient, agentKey, sid, resp, "Session:      ")
@@ -816,9 +814,8 @@ func handleInvocationResponse(
 	agentName string,
 	timeout time.Duration,
 ) error {
-	requestID := resp.Header.Get("apim-request-id")
-	if requestID != "" {
-		fmt.Printf("Trace ID: %s\n", requestID)
+	if traceID := responseTraceID(resp); traceID != "" {
+		fmt.Printf("Trace ID:     %s\n", traceID)
 	}
 
 	if resp.StatusCode >= 400 {
@@ -1125,6 +1122,23 @@ func createConversation(ctx context.Context, projectEndpoint, agentName, bearerT
 	return "", fmt.Errorf("conversation response missing 'id' field")
 }
 
+// responseTraceID returns the trace ID from the response, preferring x-request-id
+// and falling back to apim-request-id. If a header value is comma-folded (which
+// can happen when an intermediary like APIM combines duplicate headers per
+// RFC 7230 §3.2.2), the first non-empty token is returned.
+func responseTraceID(resp *http.Response) string {
+	raw := resp.Header.Get("x-request-id")
+	if raw == "" {
+		raw = resp.Header.Get("apim-request-id")
+	}
+	for part := range strings.SplitSeq(raw, ",") {
+		if id := strings.TrimSpace(part); id != "" {
+			return id
+		}
+	}
+	return ""
+}
+
 // readSSEStream reads a Server-Sent Events stream from the Foundry Responses API,
 // printing text deltas in real-time and returning the final response or any error.
 func readSSEStream(body io.Reader, agentName string) error {
diff --git a/cli/azd/extensions/azure.ai.agents/internal/cmd/invoke_test.go b/cli/azd/extensions/azure.ai.agents/internal/cmd/invoke_test.go
index 27aa72d4ab7..c7f16326ccc 100644
--- a/cli/azd/extensions/azure.ai.agents/internal/cmd/invoke_test.go
+++ b/cli/azd/extensions/azure.ai.agents/internal/cmd/invoke_test.go
@@ -1025,3 +1025,69 @@ func TestCreateConversation(t *testing.T) {
 		})
 	}
 }
+
+func TestResponseTraceID(t *testing.T) {
+	t.Parallel()
+
+	tests := []struct {
+		name    string
+		headers map[string]string
+		want    string
+	}{
+		{
+			name:    "prefers x-request-id when both present",
+			headers: map[string]string{"X-Request-ID": "trace-abc", "apim-request-id": "apim-xyz"},
+			want:    "trace-abc",
+		},
+		{
+			name:    "falls back to apim-request-id",
+			headers: map[string]string{"apim-request-id": "apim-xyz"},
+			want:    "apim-xyz",
+		},
+		{
+			name:    "returns empty when neither present",
+			headers: map[string]string{},
+			want:    "",
+		},
+		{
+			name:    "returns x-request-id when only it is present",
+			headers: map[string]string{"X-Request-ID": "trace-only"},
+			want:    "trace-only",
+		},
+		{
+			name:    "deduplicates comma-folded x-request-id",
+			headers: map[string]string{"X-Request-ID": "trace-abc,trace-abc"},
+			want:    "trace-abc",
+		},
+		{
+			name:    "returns first token when x-request-id is comma-list",
+			headers: map[string]string{"X-Request-ID": "trace-first, trace-second"},
+			want:    "trace-first",
+		},
+		{
+			name:    "skips leading empty token in comma-folded x-request-id",
+			headers: map[string]string{"X-Request-ID": ", trace-second"},
+			want:    "trace-second",
+		},
+		{
+			name:    "deduplicates comma-folded apim-request-id fallback",
+			headers: map[string]string{"apim-request-id": "apim-xyz, apim-xyz"},
+			want:    "apim-xyz",
+		},
+	}
+
+	for _, tt := range tests {
+		t.Run(tt.name, func(t *testing.T) {
+			t.Parallel()
+
+			resp := &http.Response{Header: http.Header{}}
+			for k, v := range tt.headers {
+				resp.Header.Set(k, v)
+			}
+
+			if got := responseTraceID(resp); got != tt.want {
+				t.Errorf("responseTraceID() = %q, want %q", got, tt.want)
+			}
+		})
+	}
+}