diff --git a/roles/tox/README.rst b/roles/tox/README.rst
index 89cb3a499..041d4932d 100644
--- a/roles/tox/README.rst
+++ b/roles/tox/README.rst
@@ -13,6 +13,9 @@ Runs tox for a project
    ``ALL`` runs all test environments while an empty string runs
    all test environments configured with ``envlist`` in tox.
 
+   Internally this will always be expanded into a comma separated
+   list of test environments to run.
+
 .. zuul:rolevar:: tox_executable
    :default: tox
 
diff --git a/roles/tox/library/tox_install_sibling_packages.py b/roles/tox/library/tox_install_sibling_packages.py
index 75a82eda7..0f89d29f2 100644
--- a/roles/tox/library/tox_install_sibling_packages.py
+++ b/roles/tox/library/tox_install_sibling_packages.py
@@ -32,9 +32,14 @@ requirements:
 options:
   tox_envlist:
     description:
-      - The tox environment to operate in.
+      - The tox test environments to act on.
     required: true
     type: str
+  tox_show_config:
+    description:
+      - Path to a file containing the output from C(tox --showconfig).
+    required: true
+    type: path
   project_dir:
     description:
       - The directory in which the project we care about is in.
@@ -159,19 +164,126 @@ def _get_package_root(name, sibling_packages):
     return pkg_root
 
 
+def find_installed_siblings(tox_python, package_name, sibling_python_packages):
+    installed_sibling_packages = []
+    for dep_name in get_installed_packages(tox_python):
+        log.append(
+            "Found {name} python package installed".format(
+                name=dep_name))
+        if (dep_name == package_name or
+            prAPI.to_filename(dep_name) == package_name):
+            # We don't need to re-process ourself.
+            # We've filtered ourselves from the source dir list,
+            # but let's be sure nothing is weird.
+            log.append(
+                "Skipping {name} because it's us".format(
+                    name=dep_name))
+            continue
+        if dep_name in sibling_python_packages:
+            log.append(
+                "Package {name} on system in {root}".format(
+                    name=dep_name,
+                    root=sibling_python_packages[dep_name]))
+            installed_sibling_packages.append(dep_name)
+        elif prAPI.to_filename(dep_name) in sibling_python_packages:
+            real_name = prAPI.to_filename(dep_name)
+            log.append(
+                "Package {name} ({pkg_name}) on system in {root}".format(
+                    name=dep_name,
+                    pkg_name=real_name,
+                    root=sibling_python_packages[real_name]))
+            # need to use dep_name here for later constraint file rewrite
+            installed_sibling_packages.append(dep_name)
+    return installed_sibling_packages
+
+
+def install_siblings(envdir, projects, package_name, constraints):
+    changed = False
+    tox_python = '{envdir}/bin/python'.format(envdir=envdir)
+
+    sibling_python_packages = get_sibling_python_packages(
+        projects, tox_python)
+    for name, root in sibling_python_packages.items():
+        log.append("Sibling {name} at {root}".format(name=name,
+                                                     root=root))
+
+    installed_sibling_packages = find_installed_siblings(
+        tox_python,
+        package_name,
+        sibling_python_packages)
+
+    if constraints:
+        constraints_file = write_new_constraints_file(
+            constraints, installed_sibling_packages)
+
+    for sibling_package in installed_sibling_packages:
+        changed = True
+        log.append("Uninstalling {name}".format(name=sibling_package))
+        uninstall_output = subprocess.check_output(
+            [tox_python, '-m',
+             'pip', 'uninstall', '-y', sibling_package],
+            stderr=subprocess.STDOUT)
+        log.extend(uninstall_output.decode('utf-8').split('\n'))
+
+        args = [tox_python, '-m', 'pip', 'install']
+        if constraints:
+            args.extend(['-c', constraints_file])
+
+        pkg_root = _get_package_root(sibling_package,
+                                     sibling_python_packages)
+        log.append(
+            "Installing {name} from {root} for deps".format(
+                name=sibling_package,
+                root=pkg_root))
+        args.append(pkg_root)
+
+        install_output = subprocess.check_output(args)
+        log.extend(install_output.decode('utf-8').split('\n'))
+
+    for sibling_package in installed_sibling_packages:
+        changed = True
+        pkg_root = _get_package_root(sibling_package,
+                                     sibling_python_packages)
+        log.append(
+            "Installing {name} from {root}".format(
+                name=sibling_package,
+                root=pkg_root))
+
+        install_output = subprocess.check_output(
+            [tox_python, '-m', 'pip', 'install', '--no-deps',
+             pkg_root])
+        log.extend(install_output.decode('utf-8').split('\n'))
+    return changed
+
+
 def main():
     module = AnsibleModule(
         argument_spec=dict(
             tox_envlist=dict(required=True, type='str'),
+            tox_show_config=dict(required=True, type='path'),
             tox_constraints_file=dict(type='str'),
             project_dir=dict(required=True, type='str'),
             projects=dict(required=True, type='list'),
         )
     )
-    envlist = module.params['tox_envlist']
     constraints = module.params.get('tox_constraints_file')
     project_dir = module.params['project_dir']
     projects = module.params['projects']
+    tox_envlist = module.params.get('tox_envlist', '')
+    tox_show_config = module.params.get('tox_show_config')
+
+    tox_config = configparser.ConfigParser()
+    tox_config.read(tox_show_config)
+
+    envlist = {testenv.strip() for testenv
+               in tox_envlist.split(',')}
+
+    if not envlist:
+        module.exit_json(
+            changed=False,
+            msg='No envlist to run, no action needed.')
+
+    log.append('Using envlist: {}'.format(envlist))
 
     if not os.path.exists(os.path.join(project_dir, 'setup.cfg')):
         module.exit_json(changed=False, msg="No setup.cfg, no action needed")
@@ -187,110 +299,34 @@ def main():
         module.exit_json(
             changed=False, msg="No name in setup.cfg, skipping siblings")
 
-    envdir = '{project_dir}/.tox/{envlist}'.format(
-        project_dir=project_dir, envlist=envlist)
-    if not os.path.exists(envdir):
-        module.exit_json(
-            changed=False, msg="envdir does not exist, skipping siblings")
-
-    tox_python = '{envdir}/bin/python'.format(envdir=envdir)
-    # Write a log file into the .tox dir so that it'll get picked up
-    # Name it with envlist as a prefix so that fetch-tox-output will properly
-    # get it in a multi-env scenario
-    log_dir = '{envdir}/log'.format(envdir=envdir)
-    log_file = '{log_dir}/{envlist}-siblings.txt'.format(
-        log_dir=log_dir, envlist=envlist)
-
     log.append(
         "Processing siblings for {name} from {project_dir}".format(
             name=package_name,
             project_dir=project_dir))
 
     changed = False
-
-    try:
-        sibling_python_packages = get_sibling_python_packages(
-            projects, tox_python)
-        for name, root in sibling_python_packages.items():
-            log.append("Sibling {name} at {root}".format(name=name, root=root))
-        found_sibling_packages = []
-        for dep_name in get_installed_packages(tox_python):
-            log.append(
-                "Found {name} python package installed".format(
-                    name=dep_name))
-            if (dep_name == package_name or
-                prAPI.to_filename(dep_name) == package_name):
-                # We don't need to re-process ourself. We've filtered ourselves
-                # from the source dir list, but let's be sure nothing is weird.
-                log.append(
-                    "Skipping {name} because it's us".format(
-                        name=dep_name))
-                continue
-            if dep_name in sibling_python_packages:
-                log.append(
-                    "Package {name} on system in {root}".format(
-                        name=dep_name,
-                        root=sibling_python_packages[dep_name]))
-                changed = True
-                found_sibling_packages.append(dep_name)
-            elif prAPI.to_filename(dep_name) in sibling_python_packages:
-                real_name = prAPI.to_filename(dep_name)
-                log.append(
-                    "Package {name} ({pkg_name}) on system in {root}".format(
-                        name=dep_name,
-                        pkg_name=real_name,
-                        root=sibling_python_packages[real_name]))
-                changed = True
-                # need to use dep_name here for later constraint file rewrite
-                found_sibling_packages.append(dep_name)
-
-        if constraints:
-            constraints_file = write_new_constraints_file(
-                constraints, found_sibling_packages)
-
-        for sibling_package in found_sibling_packages:
-            log.append("Uninstalling {name}".format(name=sibling_package))
-            uninstall_output = subprocess.check_output(
-                [tox_python, '-m',
-                 'pip', 'uninstall', '-y', sibling_package],
-                stderr=subprocess.STDOUT)
-            log.extend(uninstall_output.decode('utf-8').split('\n'))
-
-            args = [tox_python, '-m', 'pip', 'install']
-            if constraints:
-                args.extend(['-c', constraints_file])
-
-            pkg_root = _get_package_root(sibling_package,
-                                         sibling_python_packages)
-            log.append(
-                "Installing {name} from {root} for deps".format(
-                    name=sibling_package,
-                    root=pkg_root))
-            args.append(pkg_root)
-
-            install_output = subprocess.check_output(args)
-            log.extend(install_output.decode('utf-8').split('\n'))
-
-        for sibling_package in found_sibling_packages:
-            pkg_root = _get_package_root(sibling_package,
-                                         sibling_python_packages)
-            log.append(
-                "Installing {name} from {root}".format(
-                    name=sibling_package,
-                    root=pkg_root))
-
-            install_output = subprocess.check_output(
-                [tox_python, '-m', 'pip', 'install', '--no-deps',
-                 pkg_root])
-            log.extend(install_output.decode('utf-8').split('\n'))
-    except Exception as e:
-        tb = traceback.format_exc()
-        log.append(str(e))
-        log.append(tb)
-        module.fail_json(msg=str(e), log="\n".join(log))
-    finally:
-        log_text = "\n".join(log)
-        module.append_to_file(log_file, log_text)
+    for testenv in envlist:
+        testenv_config = tox_config['testenv:{}'.format(testenv)]
+        envdir = testenv_config['envdir']
+        envlogdir = testenv_config['envlogdir']
+        try:
+            # Write a log file into the .tox dir so that it'll get picked up
+            # Name it with testenv as a prefix so that fetch-tox-output
+            # will properly get it in a multi-env scenario
+            log_file = '{envlogdir}/{testenv}-siblings.txt'.format(
+                envlogdir=envlogdir, testenv=testenv)
+            changed = changed or install_siblings(envdir,
+                                                  projects,
+                                                  package_name,
+                                                  constraints)
+        except Exception as e:
+            tb = traceback.format_exc()
+            log.append(str(e))
+            log.append(tb)
+            module.fail_json(msg=str(e), log="\n".join(log))
+        finally:
+            log_text = "\n".join(log)
+            module.append_to_file(log_file, log_text)
     module.exit_json(changed=changed, msg=log_text)
 
 
diff --git a/roles/tox/tasks/main.yaml b/roles/tox/tasks/main.yaml
index e14741ba0..fee325608 100644
--- a/roles/tox/tasks/main.yaml
+++ b/roles/tox/tasks/main.yaml
@@ -1,8 +1,3 @@
-- name: Require tox_envlist variable
-  fail:
-    msg: tox_envlist is required for this role
-  when: tox_envlist is not defined
-
 - name: Check to see if the constraints file exists
   stat:
     path: "{{ tox_constraints_file }}"
@@ -25,6 +20,49 @@
       UPPER_CONSTRAINTS_FILE: "{{ tox_constraints_file }}"
   when: tox_constraints_file is defined
 
+# Tox siblings cannot take 'ALL' and tox_parse_output expects
+# an envlist to be supplied so always set _tox_envlist equal to
+# the list of testenvs we're going to run
+- name: Set _tox_envlist from supplied tox_envlist
+  set_fact:
+    _tox_envlist: "{{ tox_envlist }}"
+  when:
+    - tox_envlist is defined and tox_envlist
+    - tox_envlist != "ALL"
+
+- name: Get tox default envlist
+  command: "{{ tox_executable }} -l"
+  args:
+    chdir: "{{ zuul_work_dir }}"
+  register: _tox_default_envlist
+  when: tox_envlist is not defined or not tox_envlist
+
+- name: Set tox envlist fact
+  set_fact:
+    _tox_envlist: "{{ _tox_default_envlist.stdout_lines | join(',') }}"
+  when:
+    - _tox_default_envlist is defined
+    - _tox_default_envlist.stdout_lines is defined
+
+- name: Get all tox testenvs
+  command: "{{ tox_executable }} -a"
+  args:
+    chdir: "{{ zuul_work_dir }}"
+  register: _tox_all_testenvs
+  when: tox_envlist is defined and tox_envlist == 'ALL'
+
+- name: Set tox envlist fact
+  set_fact:
+    _tox_envlist: "{{ _tox_all_testenvs.stdout_lines | join(',') }}"
+  when:
+    - _tox_all_testenvs is defined
+    - _tox_all_testenvs.stdout_lines is defined
+
+- name: Fail if tox_envlist is empty
+  fail:
+    msg: "No envlist configured in zuul or tox.ini"
+  when: _tox_envlist is not defined
+
 - name: Install tox siblings
   include: siblings.yaml
   when: tox_install_siblings
@@ -33,9 +71,7 @@
   debug:
     msg: >-
       {{ tox_executable }}
-      {% if tox_envlist is defined and tox_envlist %}
-      -e{{ tox_envlist }}
-      {% endif %}
+      -e{{ _tox_envlist }}
       {{ tox_extra_args }}
 
 - block:
@@ -45,9 +81,7 @@
       environment: "{{ tox_environment|combine(tox_constraints_env|default({})) }}"
       command: >-
         {{ tox_executable }}
-        {% if tox_envlist is defined and tox_envlist %}
-        -e{{ tox_envlist }}
-        {% endif %}
+        -e{{ _tox_envlist }}
         {{ tox_extra_args }}
       register: tox_output
 
@@ -57,7 +91,7 @@
     - name: Look for output
       tox_parse_output:
         tox_output: '{{ tox_output.stdout }}'
-        tox_envlist: '{{ tox_envlist }}'
+        tox_envlist: '{{ _tox_envlist }}'
         workdir: '{{ zuul_work_dir }}'
       when: tox_inline_comments
       register: file_comments
diff --git a/roles/tox/tasks/siblings.yaml b/roles/tox/tasks/siblings.yaml
index 77c650172..65c21bc63 100644
--- a/roles/tox/tasks/siblings.yaml
+++ b/roles/tox/tasks/siblings.yaml
@@ -1,14 +1,35 @@
 # Install sibling with tox so we can replace them later
 - name: Run tox without tests
-  command: "{{ tox_executable }} --notest -e{{ tox_envlist }}"
+  command: >-
+    {{ tox_executable }}
+    --notest
+    -e{{ _tox_envlist }}
   args:
     chdir: "{{ zuul_work_dir }}"
   environment: "{{ tox_environment|combine(tox_constraints_env|default({})) }}"
 
-# TODO(mordred) handle tox_envlist being a list
+# This is needed since python < 3.2 can't parse ini files from strings
+- name: Create a tempfile to save tox showconfig
+  tempfile:
+  register: _tox_show_config_tempfile
+
+# py27, py35..py38 etc are generated on the fly if not
+# explicitly added to tox.ini, so force tox to generate
+# the config for the testenvs we're using.
+- name: Get tox envlist config
+  shell: "{{ tox_executable }} --showconfig -e {{ _tox_envlist }} > {{ _tox_show_config_tempfile.path }}"
+  args:
+    chdir: "{{ zuul_work_dir }}"
+
 - name: Install any sibling python packages
   tox_install_sibling_packages:
-    tox_envlist: "{{ tox_envlist }}"
+    tox_envlist: "{{ _tox_envlist }}"
+    tox_show_config: "{{ _tox_show_config_tempfile.path }}"
     tox_constraints_file: "{{ tox_constraints_file | default(omit) }}"
     project_dir: "{{ zuul_work_dir }}"
     projects: "{{ zuul.projects.values() | selectattr('required') | list }}"
+
+- name: Remove tempfile
+  file:
+    state: absent
+    path: "{{ _tox_show_config_tempfile.path }}"
diff --git a/test-playbooks/python/tox.ini b/test-playbooks/python/tox.ini
new file mode 100644
index 000000000..ac5f72869
--- /dev/null
+++ b/test-playbooks/python/tox.ini
@@ -0,0 +1,12 @@
+[tox]
+envlist = linters
+skipsdist = true
+
+[testenv]
+whitelist_externals = sh
+
+[testenv:linters]
+commands = sh -c "echo linters >> {posargs}"
+
+[testenv:non-default]
+commands = sh -c "echo non-default >> {posargs}"
diff --git a/test-playbooks/python/tox.yaml b/test-playbooks/python/tox.yaml
new file mode 100644
index 000000000..0658db446
--- /dev/null
+++ b/test-playbooks/python/tox.yaml
@@ -0,0 +1,78 @@
+- hosts: all
+  tasks:
+    - name: Run bindep
+      include_role:
+        name: bindep
+    - name: Run tox with constraints
+      include_role:
+        name: tox
+      vars:
+        tox_envlist: docs
+        tox_constraints_file: '{{ zuul.project.src_dir }}/zuul-tests.d/test-constraints.txt'
+
+    - name: Run tox with multiple testenvs
+      include_role:
+        name: tox
+      vars:
+        tox_envlist: docs,linters
+        tox_environment:
+          ANSIBLE_ROLES_PATH: "{{ ansible_user_dir }}/{{ zuul.project.src_dir }}/roles"
+          ANSIBLE_LIBRARY: "{{ ansible_user_dir }}/{{ zuul.project.src_dir }}/tests/fake-ansible"
+
+    - name: Create tempfile to verify testenvs ran
+      tempfile:
+      register: default_tempfile
+
+    - block:
+        - name: Run tox with empty envlist
+          include_role:
+            name: tox
+          vars:
+            zuul_work_dir: "{{ zuul.project.src_dir }}/test-playbooks/python/"
+            tox_extra_args: "{{ default_tempfile.path }}"
+            tox_install_siblings: false
+            tox_envlist: ''
+            tox_environment:
+              ANSIBLE_ROLES_PATH: "{{ ansible_user_dir }}/{{ zuul.project.src_dir }}/roles"
+              ANSIBLE_LIBRARY: "{{ ansible_user_dir }}/{{ zuul.project.src_dir }}/tests/fake-ansible"
+
+        - name: Make sure magic lines are present
+          lineinfile:
+            path: "{{ default_tempfile.path }}"
+            line: linters
+          check_mode: true
+          register: default_status
+          failed_when: default_status is changed
+      always:
+        - name: Remove tempfile
+          file:
+            state: absent
+            path: "{{ default_tempfile.path }}"
+
+    - block:
+        - name: Create tempfile to verify testenvs ran
+          tempfile:
+          register: ALL_tempfile
+
+        - name: Run tox with ALL
+          include_role:
+            name: tox
+          vars:
+            zuul_work_dir: "{{ zuul.project.src_dir }}/test-playbooks/python/"
+            tox_install_siblings: false
+            tox_extra_args: "{{ ALL_tempfile.path }}"
+            tox_envlist: 'ALL'
+            tox_environment:
+              ANSIBLE_ROLES_PATH: "{{ ansible_user_dir }}/{{ zuul.project.src_dir }}/roles"
+              ANSIBLE_LIBRARY: "{{ ansible_user_dir }}/{{ zuul.project.src_dir }}/tests/fake-ansible"
+      always:
+        - name: Make sure magic lines are present
+          loop:
+            - linters
+            - non-default
+          lineinfile:
+            path: "{{ ALL_tempfile.path }}"
+            line: "{{ item }}"
+          check_mode: true
+          register: ALL_status
+          failed_when: ALL_status is changed
diff --git a/test-playbooks/tox-siblings.yaml b/test-playbooks/tox-siblings.yaml
deleted file mode 100644
index 02a5acff7..000000000
--- a/test-playbooks/tox-siblings.yaml
+++ /dev/null
@@ -1,14 +0,0 @@
-- hosts: all
-  tasks:
-    - name: Run bindep
-      include_role:
-        name: bindep
-    - name: Run tox with constraints
-      include_role:
-        name: tox
-      vars:
-        tox_envlist: docs
-        tox_constraints_file: '{{ zuul.project.src_dir }}/zuul-tests.d/test-constraints.txt'
-        tox_environment:
-          ANSIBLE_ROLES_PATH: "{{ ansible_user_dir }}/{{ zuul.project.src_dir }}/roles"
-          ANSIBLE_LIBRARY: "{{ ansible_user_dir }}/{{ zuul.project.src_dir }}/tests/fake-ansible"
diff --git a/zuul-tests.d/python-jobs.yaml b/zuul-tests.d/python-jobs.yaml
index 961227c3d..36cf00af7 100644
--- a/zuul-tests.d/python-jobs.yaml
+++ b/zuul-tests.d/python-jobs.yaml
@@ -400,13 +400,14 @@
           label: centos-8-plain
 
 - job:
-    name: zuul-jobs-test-tox-siblings
+    name: zuul-jobs-test-tox
     description: Test the tox role's sibling functionality
     files:
       - roles/tox/.*
       - tox.ini
-      - test-playbooks/tox-siblings.yaml
-    run: test-playbooks/tox-siblings.yaml
+      - test-playbooks/python/tox.yaml
+      - test-playbooks/python/tox.ini
+    run: test-playbooks/python/tox.yaml
     required-projects:
       - zuul/zuul
       - zuul/nodepool
@@ -540,7 +541,7 @@
         - zuul-jobs-test-fetch-sphinx-tarball-ubuntu-bionic-plain
         - zuul-jobs-test-fetch-sphinx-tarball-ubuntu-xenial-plain
         - zuul-jobs-test-fetch-sphinx-tarball-centos-8-plain
-        - zuul-jobs-test-tox-siblings
+        - zuul-jobs-test-tox
         - zuul-jobs-test-fetch-tox-output
         - zuul-jobs-test-fetch-tox-output-synchronize
         - zuul-jobs-test-fetch-subunit-output
@@ -585,7 +586,7 @@
         - zuul-jobs-test-fetch-sphinx-tarball-ubuntu-bionic-plain
         - zuul-jobs-test-fetch-sphinx-tarball-ubuntu-xenial-plain
         - zuul-jobs-test-fetch-sphinx-tarball-centos-8-plain
-        - zuul-jobs-test-tox-siblings
+        - zuul-jobs-test-tox
         - zuul-jobs-test-fetch-tox-output
         - zuul-jobs-test-fetch-tox-output-synchronize
         - zuul-jobs-test-fetch-subunit-output