diff --git a/packages/server/lib/util/ts-node.js b/packages/server/lib/util/ts-node.js
index d44d07c4c0df..439bf6cb4f0c 100644
--- a/packages/server/lib/util/ts-node.js
+++ b/packages/server/lib/util/ts-node.js
@@ -27,6 +27,7 @@ const registerTsNode = (projectRoot, pluginsFile) => {
     debug('typescript path: %s', tsPath)
     debug('registering project TS with options %o', tsOptions)
 
+    require('tsconfig-paths/register')
     tsnode.register(tsOptions)
   } catch (err) {
     debug(`typescript doesn't exist. ts-node setup failed.`)
diff --git a/packages/server/package.json b/packages/server/package.json
index 11bebeedbc67..254aa0d77e0f 100644
--- a/packages/server/package.json
+++ b/packages/server/package.json
@@ -178,6 +178,7 @@
     "supertest-session": "4.0.0",
     "through2": "2.0.5",
     "ts-loader": "7.0.4",
+    "tsconfig-paths": "3.9.0",
     "webpack": "4.43.0",
     "ws": "5.2.2",
     "xvfb": "cypress-io/node-xvfb#22e3783c31d81ebe64d8c0df491ea00cdc74726a",
diff --git a/packages/server/test/e2e/1_typescript_spec_support_spec.ts b/packages/server/test/e2e/1_typescript_spec_support_spec.ts
index 82dfa6f8fdfa..8c85f5ff1ac7 100644
--- a/packages/server/test/e2e/1_typescript_spec_support_spec.ts
+++ b/packages/server/test/e2e/1_typescript_spec_support_spec.ts
@@ -29,6 +29,9 @@ describe('e2e typescript in spec and support file', function () {
     })
   })
 
+  // this covers spec/support files as well as the plugins file
+  // @see https://github.com/cypress-io/cypress/issues/7006
+  // @see https://github.com/cypress-io/cypress/issues/8555
   it('respects tsconfig paths', function () {
     return e2e.exec(this, {
       project: Fixtures.projectPath('ts-proj-with-paths'),
diff --git a/packages/server/test/support/fixtures/projects/ts-proj-with-paths/cypress.json b/packages/server/test/support/fixtures/projects/ts-proj-with-paths/cypress.json
index be9e6bf4576b..0967ef424bce 100644
--- a/packages/server/test/support/fixtures/projects/ts-proj-with-paths/cypress.json
+++ b/packages/server/test/support/fixtures/projects/ts-proj-with-paths/cypress.json
@@ -1,4 +1 @@
-{
-  "supportFile": false,
-  "pluginsFile": false
-}
+{}
diff --git a/packages/server/test/support/fixtures/projects/ts-proj-with-paths/cypress/plugins/index.ts b/packages/server/test/support/fixtures/projects/ts-proj-with-paths/cypress/plugins/index.ts
new file mode 100644
index 000000000000..037720a88e4e
--- /dev/null
+++ b/packages/server/test/support/fixtures/projects/ts-proj-with-paths/cypress/plugins/index.ts
@@ -0,0 +1,7 @@
+import { appName } from '@app/main'
+
+if (appName !== 'Best App Ever') {
+  throw new Error('Path alias not working properly in plugins file!')
+}
+
+export default () => {}
diff --git a/packages/server/test/support/fixtures/projects/ts-proj-with-paths/cypress/support/index.ts b/packages/server/test/support/fixtures/projects/ts-proj-with-paths/cypress/support/index.ts
new file mode 100644
index 000000000000..b45bd0d4b86a
--- /dev/null
+++ b/packages/server/test/support/fixtures/projects/ts-proj-with-paths/cypress/support/index.ts
@@ -0,0 +1,5 @@
+import { appName } from '@app/main'
+
+if (appName !== 'Best App Ever') {
+  throw new Error('Path alias not working properly in support file!')
+}
diff --git a/yarn.lock b/yarn.lock
index 4f6056c92a5a..a1bf08712985 100644
--- a/yarn.lock
+++ b/yarn.lock
@@ -24475,7 +24475,7 @@ tsconfig-paths-webpack-plugin@^3.3.0:
     enhanced-resolve "^4.0.0"
     tsconfig-paths "^3.4.0"
 
-tsconfig-paths@^3.4.0:
+tsconfig-paths@3.9.0, tsconfig-paths@^3.4.0:
   version "3.9.0"
   resolved "https://registry.yarnpkg.com/tsconfig-paths/-/tsconfig-paths-3.9.0.tgz#098547a6c4448807e8fcb8eae081064ee9a3c90b"
   integrity sha512-dRcuzokWhajtZWkQsDVKbWyY+jgcLC5sqJhg2PSgf4ZkH2aHPvaOY8YWGhmjb68b5qqTfasSsDO9k7RUiEmZAw==