diff --git a/Makefile b/Makefile
index a643f0ee5cecae..890328f900a55f 100644
--- a/Makefile
+++ b/Makefile
@@ -97,7 +97,7 @@ node_modules: package.json | node-version
 test: build
 	@npm run test-client
 	@npm run test-server
-	@npm run test-tests
+	@npm run test-test
 	@$(BIN)/run-all-tests
 
 lint: node_modules/eslint node_modules/eslint-plugin-react node_modules/babel-eslint mixedindentlint
diff --git a/circle.yml b/circle.yml
index 496bb9c3567744..409d1b621f2eca 100644
--- a/circle.yml
+++ b/circle.yml
@@ -2,6 +2,9 @@ machine:
   node:
     version: 5.10.1
 test:
+  pre:
+    - NODE_ENV=test make client/config/index.js:
+        parallel: true
   override:
     - npm run lint -- :
         parallel: true
@@ -10,22 +13,22 @@ test:
           - client/**/*.jsx
           - server/**/*.js
           - server/**/*.jsx
-    - NODE_ENV=test make client/config/index.js && NODE_ENV=test ./bin/run-tests:
+    - NODE_ENV=test ./bin/run-tests:
         parallel: true
         files:
           - client/**/Makefile
           - server/**/Makefile
-    - NODE_ENV=test make client/config/index.js && MOCHA_FILE=./test-results-client.xml npm run test-client -- --reporter=mocha-junit-reporter -w:
+    - MOCHA_FILE=./test-results-client.xml npm run test-client -- --reporter=mocha-junit-reporter:
         parallel: true
         files:
           - client/**/test/*.js
           - client/**/test/*.jsx
-    - NODE_ENV=test make client/config/index.js && MOCHA_FILE=./test-results-server.xml npm run test-server -- --reporter=mocha-junit-reporter -w:
+    - MOCHA_FILE=./test-results-server.xml npm run test-server -- --reporter=mocha-junit-reporter:
         parallel: true
         files:
           - server/**/test/*.js
           - server/**/test/*.jsx
-    - NODE_ENV=test make client/config/index.js && MOCHA_FILE=./test-results-tests.xml npm run test-tests -- --reporter=mocha-junit-reporter -w:
+    - MOCHA_FILE=./test-results-test.xml npm run test-test -- --reporter=mocha-junit-reporter:
         parallel: true
         files:
           - test/test/**/test/*.js
diff --git a/package.json b/package.json
index 315926373d3903..1da3c58486308e 100644
--- a/package.json
+++ b/package.json
@@ -123,9 +123,9 @@
   },
   "scripts": {
     "test": "make test",
-    "test-client": "NODE_ENV=test NODE_PATH=test:client test/runner.js",
-    "test-server": "NODE_ENV=test NODE_PATH=test:server:client test/runner.js",
-    "test-tests": "NODE_ENV=test NODE_PATH=test:test/test:client test/runner.js",
+    "test-client": "NODE_ENV=test NODE_PATH=test:client TEST_ROOT=client test/runner.js",
+    "test-server": "NODE_ENV=test NODE_PATH=test:server:client TEST_ROOT=server test/runner.js",
+    "test-test": "NODE_ENV=test NODE_PATH=test:client TEST_ROOT=test test/runner.js",
     "lint": "bin/run-lint"
   },
   "devDependencies": {
diff --git a/server/api/Makefile b/server/api/Makefile
deleted file mode 100644
index 9799e4d1e8b927..00000000000000
--- a/server/api/Makefile
+++ /dev/null
@@ -1,12 +0,0 @@
-NODE_BIN := $(shell npm bin)
-MOCHA ?= $(NODE_BIN)/mocha
-BASE_DIR := $(NODE_BIN)/../..
-NODE_PATH := ../:$(BASE_DIR)/client
-COMPILERS ?= js:babel/register
-REPORTER ?= spec
-UI ?= bdd
-
-test:
-	@NODE_PATH=$(NODE_PATH) $(MOCHA) --compilers $(COMPILERS) --reporter $(REPORTER) --ui $(UI)
-
-.PHONY: test
diff --git a/server/api/test/test.js b/server/api/test/test.js
index c41628613da96d..6202c9bbeb52c8 100644
--- a/server/api/test/test.js
+++ b/server/api/test/test.js
@@ -6,23 +6,23 @@ var expect = require( 'chai' ).expect,
 	request = require( 'superagent' ),
 	supertest = require( 'supertest' );
 
-/**
- * Internal dependencies
- */
-var config = require( 'config' ),
-	app = require( '../' )(),
-	localRequest = supertest( app );
-
 if ( process.env.NODE_ENV === 'desktop' ) {
 	describe( 'api', function() {
-		var sandbox = sinon.sandbox.create();
+		const sandbox = sinon.sandbox.create();
+		let app, config, localRequest;
+
+		before( () => {
+			config = require( 'config' );
+			app = require( '../' )();
+			localRequest = supertest( app );
+		} );
 
 		afterEach( function() {
 			sandbox.restore();
 		} );
 
 		it( 'should return package version', function( done ) {
-			var version = require( '../../../package.json' ).version
+			const version = require( '../../../package.json' ).version;
 
 			localRequest.get( '/version' )
 				.expect( 200, { version: version }, done );
diff --git a/server/tests.json b/server/tests.json
deleted file mode 100644
index 1a62bb8af998f4..00000000000000
--- a/server/tests.json
+++ /dev/null
@@ -1,14 +0,0 @@
-{
-	"config": {
-		"test": [ "parser" ]
-	},
-	"devdocs": {
-		"test": [ "index" ]
-	},
-	"i18n": {
-		"test": [ "index" ]
-	},
-	"pages": {
-		"test": [ "index" ]
-	}
-}
diff --git a/test/README.md b/test/README.md
index 1a14b49ae6e095..65bdc61b0286fa 100644
--- a/test/README.md
+++ b/test/README.md
@@ -49,7 +49,7 @@ We provide three single test runners because of different node path rules applie
 * `server/` folder
 * `test/` folder
 
-We have an `npm run` script for each of them: `npm run test-client`, `npm run test-server` and `npm run test-tests`. You can pass a filename or set of files to these scripts to isolate your test run to just your set of files.
+We have an `npm run` script for each of them: `npm run test-client`, `npm run test-server` and `npm run test-test`. You can pass a filename or set of files to these scripts to isolate your test run to just your set of files.
 
 Example for client:
 
@@ -63,7 +63,7 @@ Example for client:
 > # run single test suite from server folder
 > npm run test-server server/config/test/parser.js
 > # run single test suite from test folder
-> npm run test-tests test/helpers/use-nock/test/index.js
+> npm run test-test test/helpers/use-nock/test/index.js
 ```
 
 ### How to run specified suite or test-case
diff --git a/test/runner.js b/test/runner.js
index f79011e8835557..2c1748eb50cf56 100755
--- a/test/runner.js
+++ b/test/runner.js
@@ -1,18 +1,27 @@
 #!/usr/bin/env node
+var files;
+
 require( 'babel/register' );
 
+/**
+ * External dependencies
+ */
 const debug = require( 'debug' )( 'test-runner' ),
-	program = require( 'commander' ),
+	glob = require( 'glob' ),
 	Mocha = require( 'mocha' ),
 	path = require( 'path' ),
-	boot = require( './boot-test' ),
+	program = require( 'commander' );
+
+/**
+ * Internal dependencies
+ */
+const boot = require( './boot-test' ),
 	setup = require( './setup' );
 
 program
 	.usage( '[options] [files]' )
 	.option( '-R, --reporter <name>', 'specify the reporter to use', 'spec' )
-	.option( '-g, --grep <pattern>', 'only run tests matching <pattern>' )
-	.option( '-w, --whitelist', 'only run whitelisted tests when using a glob' );
+	.option( '-g, --grep <pattern>', 'only run tests matching <pattern>' );
 
 program.name = 'runner';
 
@@ -27,10 +36,6 @@ if ( program.grep ) {
 	mocha.grep( new RegExp( program.grep ) );
 }
 
-if ( program.whitelist ) {
-	setup.enableWhitelist();
-}
-
 if ( process.env.CIRCLECI ) {
 	debug( 'Hello Circle!' );
 	// give circle more time by default because containers are slow
@@ -41,12 +46,16 @@ if ( process.env.CIRCLECI ) {
 mocha.suite.beforeAll( boot.before );
 mocha.suite.afterAll( boot.after );
 
-// we could also discover all the tests using a glob?
-if ( program.args.length ) {
-	program.args.forEach( function( file ) {
-		setup.addFile( file );
-	} );
+// TODO: remove whitelist logic once we migrate client folder
+if ( process.env.TEST_ROOT === 'client' ) {
+	setup.enableWhitelist();
+}
+
+files = program.args;
+if ( files.length === 0 && ! process.env.CIRCLECI ) {
+	files = glob.sync( process.env.TEST_ROOT + '/**/test/*.@(js|jsx)' );
 }
+files.forEach( setup.addFile );
 
 mocha.addFile( path.join( __dirname, 'load-suite.js' ) );
 
diff --git a/test/setup.js b/test/setup.js
index f0c0fcbe3bc2dc..96e7042ae68146 100644
--- a/test/setup.js
+++ b/test/setup.js
@@ -32,7 +32,7 @@ function isFileWhitelisted( config, pathParts ) {
 	const folder = head( pathParts );
 
 	if ( config[ folder ] ) {
-		if ( folder === 'test' ) {
+		if ( folder === 'test' && Array.isArray( config[ folder ] ) ) {
 			return ( config[ folder ].indexOf( getFileName( pathParts ) ) !== false );
 		}
 
@@ -43,16 +43,6 @@ function isFileWhitelisted( config, pathParts ) {
 }
 
 function getConfig() {
-	if ( ! whitelistConfig && files.length === 0 ) {
-		// this assumes that there's a tests.json at the root of NODE_PATH
-		debug( 'No tests provided, loading whitelisted tests config.' );
-		return require( 'tests.json' );
-	}
-
-	return filesToConfig();
-}
-
-function filesToConfig() {
 	return reduce( files, ( config, file ) => {
 		const fileConfig = fileToConfig( tail( file.split( '/' ) ) );
 
@@ -67,7 +57,7 @@ function filesToConfig() {
 function fileToConfig( pathParts, folderConfig = {} ) {
 	const folder = head( pathParts );
 
-	if ( folder === 'test' ) {
+	if ( folder === 'test' && pathParts.length === 2 ) {
 		folderConfig[ folder ] = [ getFileName( pathParts ) ];
 	} else {
 		folderConfig[ folder ] = fileToConfig( tail( pathParts ) );
diff --git a/test/test/tests.json b/test/test/tests.json
deleted file mode 100644
index 766d784f3d7b99..00000000000000
--- a/test/test/tests.json
+++ /dev/null
@@ -1,10 +0,0 @@
-{
-	"helpers" : {
-		"use-i18n": {
-			"test": [ "index" ]
-		},
-		"use-nock": {
-			"test": [ "index" ]
-		}
-	}
-}