diff --git a/.gitignore b/.gitignore
index 46bc38313..927093831 100644
--- a/.gitignore
+++ b/.gitignore
@@ -5,6 +5,9 @@
 dist/
 build/
 venv/
+.venv/
+.tox/
+.python-version
 /site/
 /.cache/
 .pytest_cache/
diff --git a/.justfile b/.justfile
index c419685ed..04186b588 100644
--- a/.justfile
+++ b/.justfile
@@ -9,9 +9,10 @@
 # * frontend/.justfile – Building and running the frontend
 # * mkdocs/.justfile – Building and previewing the docs site
 # * website/.justfile – Building and previewing the React landing page
+# * .tox.justfile – Running Python tests via tox
 
-default:
-    @just --list
+# Run tests via tox
+mod tox '.tox.justfile'
 
 set allow-duplicate-recipes
 
@@ -22,3 +23,8 @@ import "frontend/.justfile"
 import "mkdocs/.justfile"
 
 import "website/.justfile"
+
+[default]
+[private]
+default:
+    @just --list --list-submodules --unsorted
diff --git a/.tox.justfile b/.tox.justfile
new file mode 100644
index 000000000..f7db5d823
--- /dev/null
+++ b/.tox.justfile
@@ -0,0 +1,44 @@
+# Keep in sync with pyproject.toml and .github/workflows/build-artifacts.yml
+supported_python_versions := '3.10,3.11,3.12,3.13,3.14'
+
+install_tox_msg := '''
+    tox is not installed; to install it using uv:
+        uv tool install tox --with tox-uv
+'''
+
+python_version_msg := '''
+    .python-version does not exist; to create (replace 3.14 with the desired version):
+        * using uv:
+            uv python pin 3.14
+        * if uv is not used:
+            echo 3.14 > .python-version
+'''
+
+[doc('''
+    Run tests using the default environment
+    The default Python version is set via .python-version file
+''')]
+[positional-arguments]
+test-default *args: _check_tox_installed
+    @if [ ! -f .python-version ]; then echo '{{python_version_msg}}' >&2; exit 1; fi
+    tox run -e default "${@}"
+
+[doc('Run tests against all supported Python versions')]
+[positional-arguments]
+test-supported *args: _check_tox_installed
+    tox run -e {{supported_python_versions}} "${@}"
+
+[doc('''
+    Run tests using the current environment (no venv isolation)
+    All dependencies must be already installed; a dummy environment is still created
+''')]
+[positional-arguments]
+test-current *args: _check_tox_installed
+    tox run -e dummy --skip-env-install "${@}"
+
+@_check_tox_installed:
+    if ! command -v 'tox' >/dev/null 2>&1; then echo '{{install_tox_msg}}' >&2; exit 1; fi
+
+[default]
+_list:
+    @just --list {{module_path()}} --unsorted
diff --git a/CONTRIBUTING.md b/CONTRIBUTING.md
index 1782025bb..4cbab5660 100644
--- a/CONTRIBUTING.md
+++ b/CONTRIBUTING.md
@@ -63,6 +63,36 @@ Use the `--runpostgres` flag to run the tests against Postgres as well:
 uv run pytest src/tests --runpostgres
 ```
 
+Alternatively, you can run tests via [tox](https://tox.wiki/) inside an isolated environment ensuring that the `dstack` package itself is built correctly and all requirements are specified and correct. tox and [just](https://just.systems/) must be already installed.
+
+* Run tests in the default environment:
+
+  ```shell
+  just tox::test-default
+  ```
+
+  The Python version of the default environment is configured via the `.python-version` file in the repo root directory. Note, the same file [is used by uv](https://docs.astral.sh/uv/concepts/python-versions/#python-version-files).
+
+* Run tests against all currently supported Python versions:
+
+  ```shell
+  just tox::test-supported
+  ```
+
+* Run tests in the _current_ environment:
+
+  ```shell
+  just tox::test-current
+  ```
+
+  It saves about 30-60 seconds at the cost of Python environment isolation (defeating the core purpose of tox) — no packages are built or installed, and, as a consequence, all dependencies must be already installed, but, unlike the plain pytest command, the process environment variables are still isolated.
+
+It's possible to pass pytest arguments after the `--` separator (the arguments _before_ the separator are `tox run` arguments):
+
+```shell
+just tox::test-default -- -vvv --last-failed
+```
+
 ## Add a new backend
 
 If you'd like to integrate a new cloud provider to `dstack`, follow [contributing/BACKENDS.md](contributing/BACKENDS.md).
diff --git a/pyproject.toml b/pyproject.toml
index 60b233223..818082fc4 100644
--- a/pyproject.toml
+++ b/pyproject.toml
@@ -145,9 +145,38 @@ filterwarnings = [
     "ignore:^The @wait_container_is_ready decorator:DeprecationWarning",
 ]
 
+[tool.tox]
+env_list = ["default"]
+
+[tool.tox.env_run_base]
+description = "Run tests under {base_python}"
+extras = ["all"]
+dependency_groups = ["test"]
+commands = [["pytest", { replace = "posargs", extend = true }]]
+
+# `tox run [-e default]` -- run tests inside an isolated environment
+# with Python version read from `.python-version` file
+[tool.tox.env.default]
+base_python_file = [".python-version"]
+
+# `tox run -e dummy --skip-env-install` -- run tests inside the current environment
+# all dependencies must be already installed; a dummy environment is still created
+[tool.tox.env.dummy]
+description = "Run tests inside the current environment"
+# Must be called with --skip-env-install
+dependency_groups = ["nonexistent-group-to-trigger-failure"]
+allowlist_externals = ["pytest"]
+
 [dependency-groups]
 dev = [
     "pre-commit>=4.2.0",
+    "ruff==0.12.7",  # should match .pre-commit-config.yaml
+    "pyinstrument>=5.0.0",
+    "kubernetes-stubs-elephant-fork>=35.0.0.post3",
+    {include-group = "test"},
+    {include-group = "docs"},
+]
+test = [
     "pytest~=8.0",
     "pytest-asyncio>=0.25.2",
     "pytest-mock>=3.14.0",
@@ -155,16 +184,12 @@ dev = [
     "pytest-socket>=0.7.0",
     "pytest-env>=1.1.0",
     "pytest-unordered>=0.7.0",
-    "httpbin>=0.10.2", # indirect to make compatible with Werkzeug 3
+    "pytest-xdist>=3.6.1",
     "requests-mock>=1.12.1",
-    "openai>=1.68.2",
     "freezegun>=1.5.1",
-    "ruff==0.12.7",  # should match .pre-commit-config.yaml
+    "httpbin>=0.10.2", # indirect to make compatible with Werkzeug 3
+    "openai>=1.68.2",
     "testcontainers>=4.9.2",
-    "pytest-xdist>=3.6.1",
-    "pyinstrument>=5.0.0",
-    "kubernetes-stubs-elephant-fork>=35.0.0.post3",
-    {include-group = "docs"},
 ]
 docs = [
     "dstack[server]",