diff --git a/docs/changelog/3598.bugfix.rst b/docs/changelog/3598.bugfix.rst
new file mode 100644
index 000000000..f1ee47ffa
--- /dev/null
+++ b/docs/changelog/3598.bugfix.rst
@@ -0,0 +1,6 @@
+The :func:`tox_extend_envs() hook <tox.plugin.spec.tox_extend_envs>`
+recently added in :pull:`3591` turned out to not work well with
+``tox run``. It was fixed internally, not to exhaust the underlying
+iterator on the first use.
+
+-- by :user:`webknjaz`
diff --git a/src/tox/config/main.py b/src/tox/config/main.py
index ff264ea21..9fbd9f4bc 100644
--- a/src/tox/config/main.py
+++ b/src/tox/config/main.py
@@ -2,7 +2,7 @@
 
 import os
 from collections import OrderedDict, defaultdict
-from itertools import chain
+from itertools import chain, tee
 from pathlib import Path
 from typing import TYPE_CHECKING, Any, Iterable, Iterator, Sequence, TypeVar
 
@@ -81,7 +81,11 @@ def src_path(self) -> Path:
 
     def __iter__(self) -> Iterator[str]:
         """:return: an iterator that goes through existing environments"""
-        return chain(self._src.envs(self.core), self._extra_envs)
+        # NOTE: `tee(self._extra_envs)[1]` is necessary for compatibility with
+        # NOTE: Python 3.11 and older versions. Once Python 3.12 is the lowest
+        # NOTE: supported version, it can be changed to
+        # NOTE: `chain.from_iterable(tee(self._extra_envs, 1))`.
+        return chain(self._src.envs(self.core), tee(self._extra_envs)[1])
 
     def sections(self) -> Iterator[Section]:
         yield from self._src.sections()
diff --git a/src/tox/session/state.py b/src/tox/session/state.py
index 6b63f39da..3f59ecd73 100644
--- a/src/tox/session/state.py
+++ b/src/tox/session/state.py
@@ -1,7 +1,7 @@
 from __future__ import annotations
 
 import sys
-from itertools import chain
+from itertools import chain, tee
 from typing import TYPE_CHECKING, Sequence
 
 from tox.config.main import Config
@@ -20,7 +20,7 @@ class State:
     """Runtime state holder."""
 
     def __init__(self, options: Options, args: Sequence[str]) -> None:
-        extended_envs = chain.from_iterable(MANAGER.tox_extend_envs())
+        (extended_envs,) = tee(chain.from_iterable(MANAGER.tox_extend_envs()), 1)
         self.conf = Config.make(options.parsed, options.pos_args, options.source, extended_envs)
         self.conf.core.add_constant(
             keys=["on_platform"],
diff --git a/tests/plugin/test_inline.py b/tests/plugin/test_inline.py
index 4fae64b27..46af969a3 100644
--- a/tests/plugin/test_inline.py
+++ b/tests/plugin/test_inline.py
@@ -1,5 +1,6 @@
 from __future__ import annotations
 
+import sys
 from typing import TYPE_CHECKING
 
 if TYPE_CHECKING:
@@ -43,6 +44,7 @@ def tox_extend_envs() -> tuple[str]:
         def tox_add_core_config(core_conf: ConfigSet, state: State) -> None:  # noqa: ARG001
             in_memory_config_loader = MemoryLoader(
                 base=["sentinel-base"],
+                commands_pre=["sentinel-cmd"],
                 description="sentinel-description",
             )
             state.conf.memory_seed_loaders[env_name].append(
@@ -59,3 +61,15 @@ def tox_add_core_config(core_conf: ConfigSet, state: State) -> None:  # noqa: AR
     tox_config_result = project.run("config", "-e", "sentinel-env-name", "-qq")
     tox_config_result.assert_success()
     assert "base = sentinel-base" in tox_config_result.out
+
+    tox_run_result = project.run("run", "-e", "sentinel-env-name", "-q")
+    tox_run_result.assert_failed()
+    underlying_expected_oserror_msg = (
+        "[WinError 2] The system cannot find the file specified"
+        if sys.platform == "win32"
+        else "[Errno 2] No such file or directory: 'sentinel-cmd'"
+    )
+    expected_cmd_lookup_error_txt = (
+        f"sentinel-env-name: Exception running subprocess {underlying_expected_oserror_msg!s}\n"
+    )
+    assert expected_cmd_lookup_error_txt in tox_run_result.out