diff --git a/common/changes/@rushstack/debug-certificate-manager/bmiddha-certificatestore-homedir_2025-08-22-20-14.json b/common/changes/@rushstack/debug-certificate-manager/bmiddha-certificatestore-homedir_2025-08-22-20-14.json
new file mode 100644
index 00000000000..1df91879e11
--- /dev/null
+++ b/common/changes/@rushstack/debug-certificate-manager/bmiddha-certificatestore-homedir_2025-08-22-20-14.json
@@ -0,0 +1,10 @@
+{
+  "changes": [
+    {
+      "packageName": "@rushstack/debug-certificate-manager",
+      "comment": "Fix handling of home directory paths when reading debug-certificate-manager.json config file.",
+      "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 246b2793705..71b1dfbdfa6 100644
--- a/libraries/debug-certificate-manager/src/CertificateStore.ts
+++ b/libraries/debug-certificate-manager/src/CertificateStore.ts
@@ -69,6 +69,9 @@ export class CertificateStore {
           debugCertificateManagerConfig = JSON.parse(configContent) as ICertificateStoreOptions;
           if (debugCertificateManagerConfig.storePath) {
             storePath = path.resolve(currentDir, debugCertificateManagerConfig.storePath);
+            if (storePath.startsWith('~')) {
+              storePath = path.join(homedir(), storePath.slice(2));
+            }
           }
         }
         const parentDir: string | undefined = path.dirname(currentDir);