diff --git a/src/dstack/_internal/server/services/jobs/configurators/base.py b/src/dstack/_internal/server/services/jobs/configurators/base.py
index 0e770b2e90..72821f1dd3 100644
--- a/src/dstack/_internal/server/services/jobs/configurators/base.py
+++ b/src/dstack/_internal/server/services/jobs/configurators/base.py
@@ -220,6 +220,17 @@ def _dstack_image_commands(self) -> List[str]:
         ):
             return []
         return [
+            f"eval $(echo 'export DSTACK_VENV_DIR={DSTACK_DIR}/venv' | sudo tee -a {DSTACK_PROFILE_PATH})",
+            # Make sure /dstack/venv is owned by the current user.
+            # XXX: Generally, /dstack and all its descendants should be owned by root, as it is
+            # intended to be a place for files shared by all users, but since a non-root user
+            # should be able to install packages via pip and we want to avoid cluttering the user's
+            # home dir if possible, we make the venv dir owned by the current user rather than
+            # creating it inside the user's home or (even worse) making /dstack/venv
+            # world-writable.
+            "sudo rm -rf $DSTACK_VENV_DIR",
+            "sudo mkdir $DSTACK_VENV_DIR",
+            "sudo chown $(id -u):$(id -g) $DSTACK_VENV_DIR",
             # `uv` may emit:
             # > warning: `VIRTUAL_ENV=/dstack/venv` does not match the project environment path
             # > `.venv` and will be ignored; use `--active` to target the active environment
@@ -228,9 +239,8 @@ def _dstack_image_commands(self) -> List[str]:
             # used for legacy `pip`-based configurations). `--no-active` suppresses the warning.
             # Alternatively, the user can call `deactivate` once before using `uv`.
             # If the user really wants to reuse dstack's venv, they must spefify `--active`.
-            f"uv venv -q --prompt dstack -p {self._python()} --seed {DSTACK_DIR}/venv",
-            f"echo '. {DSTACK_DIR}/venv/bin/activate' >> {DSTACK_PROFILE_PATH}",
-            f". {DSTACK_DIR}/venv/bin/activate",
+            f"uv venv -q --prompt dstack -p {self._python()} --seed $DSTACK_VENV_DIR",
+            f"eval $(echo '. $DSTACK_VENV_DIR/bin/activate' | sudo tee -a {DSTACK_PROFILE_PATH})",
         ]
 
     def _app_specs(self) -> List[AppSpec]:
diff --git a/src/tests/_internal/server/routers/test_runs.py b/src/tests/_internal/server/routers/test_runs.py
index 5f5037c79d..4f3ab2ed2d 100644
--- a/src/tests/_internal/server/routers/test_runs.py
+++ b/src/tests/_internal/server/routers/test_runs.py
@@ -115,9 +115,12 @@ def get_dev_env_run_plan_dict(
             "-i",
             "-c",
             (
-                "uv venv -q --prompt dstack -p 3.13 --seed /dstack/venv"
-                " && echo '. /dstack/venv/bin/activate' >> /dstack/profile"
-                " && . /dstack/venv/bin/activate"
+                "eval $(echo 'export DSTACK_VENV_DIR=/dstack/venv' | sudo tee -a /dstack/profile)"
+                " && sudo rm -rf $DSTACK_VENV_DIR"
+                " && sudo mkdir $DSTACK_VENV_DIR"
+                " && sudo chown $(id -u):$(id -g) $DSTACK_VENV_DIR"
+                " && uv venv -q --prompt dstack -p 3.13 --seed $DSTACK_VENV_DIR"
+                " && eval $(echo '. $DSTACK_VENV_DIR/bin/activate' | sudo tee -a /dstack/profile)"
                 " && (echo 'pip install ipykernel...'"
                 " && pip install -q --no-cache-dir ipykernel 2> /dev/null)"
                 " || echo 'no pip, ipykernel was not installed'"
@@ -344,9 +347,12 @@ def get_dev_env_run_dict(
             "-i",
             "-c",
             (
-                "uv venv -q --prompt dstack -p 3.13 --seed /dstack/venv"
-                " && echo '. /dstack/venv/bin/activate' >> /dstack/profile"
-                " && . /dstack/venv/bin/activate"
+                "eval $(echo 'export DSTACK_VENV_DIR=/dstack/venv' | sudo tee -a /dstack/profile)"
+                " && sudo rm -rf $DSTACK_VENV_DIR"
+                " && sudo mkdir $DSTACK_VENV_DIR"
+                " && sudo chown $(id -u):$(id -g) $DSTACK_VENV_DIR"
+                " && uv venv -q --prompt dstack -p 3.13 --seed $DSTACK_VENV_DIR"
+                " && eval $(echo '. $DSTACK_VENV_DIR/bin/activate' | sudo tee -a /dstack/profile)"
                 " && (echo 'pip install ipykernel...'"
                 " && pip install -q --no-cache-dir ipykernel 2> /dev/null)"
                 " || echo 'no pip, ipykernel was not installed'"
diff --git a/src/tests/_internal/server/services/jobs/configurators/test_task.py b/src/tests/_internal/server/services/jobs/configurators/test_task.py
index 6397c40e2c..3c80bf226f 100644
--- a/src/tests/_internal/server/services/jobs/configurators/test_task.py
+++ b/src/tests/_internal/server/services/jobs/configurators/test_task.py
@@ -98,10 +98,15 @@ async def test_with_commands_no_image(self, shell: Optional[str], expected_shell
             expected_shell,
             "-i",
             "-c",
-            "uv venv -q --prompt dstack -p 3.12 --seed /dstack/venv"
-            " && echo '. /dstack/venv/bin/activate' >> /dstack/profile"
-            " && . /dstack/venv/bin/activate"
-            " && sleep inf",
+            (
+                "eval $(echo 'export DSTACK_VENV_DIR=/dstack/venv' | sudo tee -a /dstack/profile)"
+                " && sudo rm -rf $DSTACK_VENV_DIR"
+                " && sudo mkdir $DSTACK_VENV_DIR"
+                " && sudo chown $(id -u):$(id -g) $DSTACK_VENV_DIR"
+                " && uv venv -q --prompt dstack -p 3.12 --seed $DSTACK_VENV_DIR"
+                " && eval $(echo '. $DSTACK_VENV_DIR/bin/activate' | sudo tee -a /dstack/profile)"
+                " && sleep inf"
+            ),
         ]
 
     async def test_no_commands(self, image_config_mock: ImageConfig):