diff --git a/common/changes/@rushstack/debug-certificate-manager/bmiddha-debug-certificate-manager-homedir-fix_2025-08-28-04-41.json b/common/changes/@rushstack/debug-certificate-manager/bmiddha-debug-certificate-manager-homedir-fix_2025-08-28-04-41.json
new file mode 100644
index 00000000000..ddc415d5cd2
--- /dev/null
+++ b/common/changes/@rushstack/debug-certificate-manager/bmiddha-debug-certificate-manager-homedir-fix_2025-08-28-04-41.json
@@ -0,0 +1,10 @@
+{
+  "changes": [
+    {
+      "packageName": "@rushstack/debug-certificate-manager",
+      "comment": "Fix homedir resolution in CertificateStore",
+      "type": "patch"
+    }
+  ],
+  "packageName": "@rushstack/debug-certificate-manager"
+}
\ No newline at end of file
diff --git a/libraries/debug-certificate-manager/src/CertificateStore.ts b/libraries/debug-certificate-manager/src/CertificateStore.ts
index 71b1dfbdfa6..19f7f0857b6 100644
--- a/libraries/debug-certificate-manager/src/CertificateStore.ts
+++ b/libraries/debug-certificate-manager/src/CertificateStore.ts
@@ -68,9 +68,11 @@ export class CertificateStore {
           const configContent: string = FileSystem.readFile(debugCertificateManagerConfigFile);
           debugCertificateManagerConfig = JSON.parse(configContent) as ICertificateStoreOptions;
           if (debugCertificateManagerConfig.storePath) {
-            storePath = path.resolve(currentDir, debugCertificateManagerConfig.storePath);
+            storePath = debugCertificateManagerConfig.storePath;
             if (storePath.startsWith('~')) {
               storePath = path.join(homedir(), storePath.slice(2));
+            } else {
+              storePath = path.resolve(currentDir, debugCertificateManagerConfig.storePath);
             }
           }
         }