diff --git a/extension/src/dcp/types.ts b/extension/src/dcp/types.ts
index e76e7f3bc21..7c93ec2b6be 100644
--- a/extension/src/dcp/types.ts
+++ b/extension/src/dcp/types.ts
@@ -1,5 +1,6 @@
 import * as vscode from 'vscode';
 import { AspireDebugSession } from '../debugger/AspireDebugSession';
+import { ServerReadyAction } from '../debugger/launchProfiles';
 
 export interface ErrorResponse {
     error: ErrorDetails;
@@ -110,6 +111,7 @@ export interface AspireResourceExtendedDebugConfiguration extends vscode.DebugCo
     runId: string;
     debugSessionId: string | null;
     projectFile?: string;
+    serverReadyAction?: ServerReadyAction;
 }
 
 export interface AspireExtendedDebugConfiguration extends vscode.DebugConfiguration {
diff --git a/extension/src/debugger/languages/dotnet.ts b/extension/src/debugger/languages/dotnet.ts
index d7f50e9c076..3650cb7781d 100644
--- a/extension/src/debugger/languages/dotnet.ts
+++ b/extension/src/debugger/languages/dotnet.ts
@@ -291,7 +291,7 @@ export function createProjectDebuggerExtension(dotNetServiceProducer: (debugSess
             // The apphost's application URL is the Aspire dashboard URL. We already get the dashboard login URL later on,
             // so we should just avoid setting up serverReadyAction and manually open the browser ourselves.
             if (!launchOptions.isApphost) {
-                debugConfiguration.serverReadyAction = determineServerReadyAction(baseProfile?.launchBrowser, baseProfile?.applicationUrl);
+                debugConfiguration.serverReadyAction = determineServerReadyAction(baseProfile?.launchBrowser, baseProfile?.applicationUrl, debugConfiguration.serverReadyAction);
             }
 
             // Temporarily disable GH Copilot on the dashboard before the extension implementation is approved
diff --git a/extension/src/debugger/launchProfiles.ts b/extension/src/debugger/launchProfiles.ts
index d08cfe6f0c8..c80b5f33fe2 100644
--- a/extension/src/debugger/launchProfiles.ts
+++ b/extension/src/debugger/launchProfiles.ts
@@ -50,7 +50,14 @@ export async function readLaunchSettings(projectPath: string): Promise<LaunchSet
             launchSettingsPath = path.join(projectDir, 'Properties', 'launchSettings.json');
         }
 
-        if (!fs.existsSync(launchSettingsPath)) {
+        const launchSettingsExists = fs.existsSync(launchSettingsPath);
+        extensionLogOutputChannel.debug('[launchSettings] Resolved launchSettings path', {
+            projectPath,
+            resolvedPath: launchSettingsPath,
+            exists: launchSettingsExists,
+        });
+
+        if (!launchSettingsExists) {
             extensionLogOutputChannel.debug(`Launch settings file not found at: ${launchSettingsPath}`);
             return null;
         }
@@ -60,6 +67,9 @@ export async function readLaunchSettings(projectPath: string): Promise<LaunchSet
         content = stripComments(content);
         const launchSettings = JSON.parse(content) as LaunchSettings;
 
+        const profileNames = launchSettings?.profiles ? Object.keys(launchSettings.profiles) : [];
+        extensionLogOutputChannel.debug(`[launchSettings] parsed ${profileNames.length} profiles: ${profileNames.join(', ')}`);
+
         extensionLogOutputChannel.debug(`Successfully read launch settings from: ${launchSettingsPath}`);
         return launchSettings;
     } catch (error) {
@@ -75,6 +85,14 @@ export function determineBaseLaunchProfile(
     launchConfig: ProjectLaunchConfiguration,
     launchSettings: LaunchSettings | null
 ): LaunchProfileResult {
+    const debugMessage =
+        `[launchProfile] determineBaseLaunchProfile:
+  disable_launch_profile=${!!launchConfig.disable_launch_profile}
+  launch_profile='${launchConfig.launch_profile ?? ''}'
+  hasLaunchSettings=${!!launchSettings}
+  profileCount=${launchSettings?.profiles ? Object.keys(launchSettings.profiles).length : 0}`;
+    extensionLogOutputChannel.debug(debugMessage);
+
     // If disable_launch_profile property is set to true in project launch configuration, there is no base profile, regardless of the value of launch_profile property.
     if (launchConfig.disable_launch_profile === true) {
         extensionLogOutputChannel.debug('Launch profile disabled via disable_launch_profile=true');
@@ -195,14 +213,23 @@ export function determineWorkingDirectory(
     return projectDir;
 }
 
-interface ServerReadyAction {
+export interface ServerReadyAction {
     action: "openExternally";
-    pattern: "\\bNow listening on:\\s+https?://\\S+";
+    pattern: string;
     uriFormat: string;
 }
 
-export function determineServerReadyAction(launchBrowser?: boolean, applicationUrl?: string): ServerReadyAction | undefined {
-    if (!launchBrowser || !applicationUrl) {
+export function determineServerReadyAction(launchBrowser?: boolean, applicationUrl?: string, debugConfigurationServerReadyAction?: ServerReadyAction): ServerReadyAction | undefined {
+    if (launchBrowser === false) {
+        return undefined;
+    }
+    
+    // A serverReadyAction may already have been defined in the aspire launch configuration. In that case, it applies to all resources unless launchBrowser is false (resource explicitly has opted out of browser launch).
+    if (debugConfigurationServerReadyAction) {
+        return debugConfigurationServerReadyAction;
+    }
+
+    if (launchBrowser === undefined || !applicationUrl) {
         return undefined;
     }
 
@@ -210,7 +237,7 @@ export function determineServerReadyAction(launchBrowser?: boolean, applicationU
 
     return {
         action: "openExternally",
-        pattern: "\\bNow listening on:\\s+https?://\\S+",
+        pattern: "\\bNow listening on:\\s+(https?://\\S+)",
         uriFormat: uriFormat
     };
 }
diff --git a/extension/src/test/dotnetDebugger.test.ts b/extension/src/test/dotnetDebugger.test.ts
index cca8f256933..9dda8982823 100644
--- a/extension/src/test/dotnetDebugger.test.ts
+++ b/extension/src/test/dotnetDebugger.test.ts
@@ -178,11 +178,13 @@ suite('Dotnet Debugger Extension Tests', () => {
         assert.strictEqual(debugConfig.executablePath, 'exePath');
         assert.strictEqual(debugConfig.checkForDevCert, true);
 
-        // serverReadyAction should be present with the applicationUrl
+        // serverReadyAction should be present when launchBrowser is true
         assert.notStrictEqual(debugConfig.serverReadyAction, undefined);
-        assert.strictEqual(debugConfig.serverReadyAction.uriFormat, 'https://localhost:5001');
+        assert.strictEqual(debugConfig.serverReadyAction?.uriFormat, 'https://localhost:5001');
+        assert.strictEqual(debugConfig.serverReadyAction?.pattern, '\\bNow listening on:\\s+(https?://\\S+)');
 
         // cleanup
         fs.rmSync(tempDir, { recursive: true, force: true });
     });
+
 });
diff --git a/extension/src/test/launchProfiles.test.ts b/extension/src/test/launchProfiles.test.ts
index 2a04c153294..a63f3f1459a 100644
--- a/extension/src/test/launchProfiles.test.ts
+++ b/extension/src/test/launchProfiles.test.ts
@@ -86,8 +86,8 @@ suite('Launch Profile Tests', () => {
 
             const result = determineBaseLaunchProfile(launchConfig, sampleLaunchSettings);
 
-            assert.strictEqual(result.profile, null);
-            assert.strictEqual(result.profileName, null);
+                assert.strictEqual(result.profile, null);
+                assert.strictEqual(result.profileName, null);
         });
 
         test('returns first profile with commandName=Project when no explicit profile specified', () => {
@@ -335,17 +335,22 @@ suite('Launch Profile Tests', () => {
     });
 
     suite('determineWorkingDirectory', () => {
-        const projectPath = path.join('C:', 'project', 'MyApp.csproj');
+        // Keep these tests cross-platform by deriving the platform's root from the current process.
+        // On Windows this is typically something like "C:\\" (drive-dependent), and on POSIX it's "/".
+        const systemRoot = path.parse(process.cwd()).root;
+        const projectPath = path.join(systemRoot, 'project', 'MyApp.csproj');
+        const projectDir = path.dirname(projectPath);
+        const absoluteWorkingDir = path.join(systemRoot, 'custom', 'working', 'dir');
 
         test('uses absolute working directory from launch profile', () => {
             const baseProfile: LaunchProfile = {
                 commandName: 'Project',
-                workingDirectory: path.join('C:', 'custom', 'working', 'dir')
+                workingDirectory: absoluteWorkingDir
             };
 
             const result = determineWorkingDirectory(projectPath, baseProfile);
 
-            assert.strictEqual(result, path.join('C:', 'custom', 'working', 'dir'));
+            assert.strictEqual(result, absoluteWorkingDir);
         });
 
         test('resolves relative working directory from launch profile', () => {
@@ -356,7 +361,7 @@ suite('Launch Profile Tests', () => {
 
             const result = determineWorkingDirectory(projectPath, baseProfile);
 
-            assert.strictEqual(result, path.join('C:', 'project', 'custom'));
+            assert.strictEqual(result, path.join(projectDir, 'custom'));
         });
 
         test('uses project directory when no working directory specified', () => {
@@ -366,13 +371,13 @@ suite('Launch Profile Tests', () => {
 
             const result = determineWorkingDirectory(projectPath, baseProfile);
 
-            assert.strictEqual(result, path.join('C:', 'project'));
+            assert.strictEqual(result, projectDir);
         });
 
         test('uses project directory when base profile is null', () => {
             const result = determineWorkingDirectory(projectPath, null);
 
-            assert.strictEqual(result, path.join('C:', 'project'));
+            assert.strictEqual(result, projectDir);
         });
     });
 
@@ -382,8 +387,34 @@ suite('Launch Profile Tests', () => {
             assert.strictEqual(result, undefined);
         });
 
-        test('returns undefined when applicationUrl is undefined', () => {
-            const result = determineServerReadyAction(true, undefined);
+        test('returns undefined when applicationUrl is undefined and no launch config serverReadyAction', () => {
+            const result = determineServerReadyAction(true, undefined, undefined);
+            assert.strictEqual(result, undefined);
+        });
+
+        test('returns existing when launchBrowser is undefined, applicationUrl is undefined and existing launch config serverReadyAction', () => {
+            const result = determineServerReadyAction(undefined, undefined, { action: 'openExternally', uriFormat: 'https://localhost:5001', pattern: '\\bNow listening on:\\s+(https?://\\S+)' });
+            assert.notStrictEqual(result, undefined);
+            assert.strictEqual(result?.action, 'openExternally');
+            assert.strictEqual(result?.uriFormat, 'https://localhost:5001');
+            assert.strictEqual(result?.pattern, '\\bNow listening on:\\s+(https?://\\S+)');
+        });
+
+        test('returns existing when launchBrowser is true, applicationUrl is undefined and existing launch config serverReadyAction', () => {
+            const result = determineServerReadyAction(true, undefined, { action: 'openExternally', uriFormat: 'https://localhost:5001', pattern: '\\bNow listening on:\\s+(https?://\\S+)' });
+            assert.notStrictEqual(result, undefined);
+            assert.strictEqual(result?.action, 'openExternally');
+            assert.strictEqual(result?.uriFormat, 'https://localhost:5001');
+            assert.strictEqual(result?.pattern, '\\bNow listening on:\\s+(https?://\\S+)');
+        });
+
+        test('returns undefined when launchBrowser is false, applicationUrl is undefined and existing launch config serverReadyAction', () => {
+            const result = determineServerReadyAction(false, undefined, { action: 'openExternally', uriFormat: 'https://localhost:5001', pattern: '\\bNow listening on:\\s+(https?://\\S+)' });
+            assert.strictEqual(result, undefined);
+        });
+
+        test('returns undefined when launchBrowser is false, applicationUrl is not undefined and existing launch config serverReadyAction', () => {
+            const result = determineServerReadyAction(false, 'https://localhost:5001', { action: 'openExternally', uriFormat: 'https://localhost:5001', pattern: '\\bNow listening on:\\s+(https?://\\S+)' });
             assert.strictEqual(result, undefined);
         });
 
@@ -394,7 +425,7 @@ suite('Launch Profile Tests', () => {
             assert.notStrictEqual(result, undefined);
             assert.strictEqual(result?.action, 'openExternally');
             assert.strictEqual(result?.uriFormat, applicationUrl);
-            assert.strictEqual(result?.pattern, '\\bNow listening on:\\s+https?://\\S+');
+            assert.strictEqual(result?.pattern, '\\bNow listening on:\\s+(https?://\\S+)');
         });
 
         test('returns serverReadyAction with first URL when multiple URLs separated by semicolon', () => {
@@ -404,7 +435,7 @@ suite('Launch Profile Tests', () => {
             assert.notStrictEqual(result, undefined);
             assert.strictEqual(result?.action, 'openExternally');
             assert.strictEqual(result?.uriFormat, 'https://localhost:5001');
-            assert.strictEqual(result?.pattern, '\\bNow listening on:\\s+https?://\\S+');
+            assert.strictEqual(result?.pattern, '\\bNow listening on:\\s+(https?://\\S+)');
         });
     });