diff --git a/src/python/pants/backend/python/util_rules/pex.py b/src/python/pants/backend/python/util_rules/pex.py
index fb0bc1c6c25..a192f2fe35a 100644
--- a/src/python/pants/backend/python/util_rules/pex.py
+++ b/src/python/pants/backend/python/util_rules/pex.py
@@ -706,7 +706,7 @@ def _create_venv_script(
         target_venv_executable = shlex.quote(str(venv_executable))
         venv_dir = shlex.quote(str(self.venv_dir))
         execute_pex_args = " ".join(
-            shlex.quote(arg)
+            f"$(ensure_absolute {shlex.quote(arg)})"
             for arg in self.complete_pex_env.create_argv(self.pex.name, python=self.pex.python)
         )
 
@@ -736,7 +736,7 @@ def _create_venv_script(
             export {" ".join(env_vars)}
             export PEX_ROOT="$(ensure_absolute ${{PEX_ROOT}})"
 
-            execute_pex_args="$(ensure_absolute {execute_pex_args})"
+            execute_pex_args="{execute_pex_args}"
             target_venv_executable="$(ensure_absolute {target_venv_executable})"
             venv_dir="$(ensure_absolute {venv_dir})"
 
@@ -789,6 +789,7 @@ class VenvPex:
     pex: Script
     python: Script
     bin: FrozenDict[str, Script]
+    venv_rel_dir: str
 
 
 @frozen_after_init
@@ -880,6 +881,7 @@ async def create_venv_pex(
         pex=pex.script,
         python=python.script,
         bin=FrozenDict((bin_name, venv_script.script) for bin_name, venv_script in scripts.items()),
+        venv_rel_dir=venv_rel_dir.as_posix(),
     )
 
 
diff --git a/src/python/pants/backend/python/util_rules/pex_test.py b/src/python/pants/backend/python/util_rules/pex_test.py
index 8bb394cd550..e6d3dca81d8 100644
--- a/src/python/pants/backend/python/util_rules/pex_test.py
+++ b/src/python/pants/backend/python/util_rules/pex_test.py
@@ -37,8 +37,9 @@
 from pants.backend.python.util_rules.pex_cli import PexPEX
 from pants.engine.fs import EMPTY_DIGEST, CreateDigest, Digest, Directory, FileContent
 from pants.engine.internals.scheduler import ExecutionError
-from pants.engine.process import Process, ProcessResult
+from pants.engine.process import Process, ProcessCacheScope, ProcessResult
 from pants.testutil.rule_runner import QueryRule, RuleRunner
+from pants.util.dirutil import safe_rmtree
 
 
 @dataclass(frozen=True)
@@ -331,9 +332,32 @@ def test_pex_working_directory(rule_runner: RuleRunner, pex_type: type[Pex | Ven
                     description="Run the pex and check its cwd",
                     working_directory=working_dir,
                     input_digest=runtime_files,
+                    # We skip the process cache for this PEX to ensure that it re-runs.
+                    cache_scope=ProcessCacheScope.PER_SESSION,
                 )
             ],
         )
+
+        # For VenvPexes, run the PEX twice while clearing the venv dir in between. This emulates
+        # situations where a PEX creation hits the process cache, while venv seeding misses the PEX
+        # cache.
+        if isinstance(pex, VenvPex):
+            # Request once to ensure that the directory is seeded, and then start a new session so that
+            # the second run happens as well.
+            _ = rule_runner.request(ProcessResult, [process])
+            rule_runner.new_session("re-run-for-venv-pex")
+            rule_runner.set_options(
+                ["--backend-packages=pants.backend.python"],
+                env_inherit={"PATH", "PYENV_ROOT", "HOME"},
+            )
+            # Clear the cache.
+            named_caches_dir = (
+                rule_runner.options_bootstrapper.bootstrap_options.for_global_scope().named_caches_dir
+            )
+            venv_dir = os.path.join(named_caches_dir, "pex_root", pex.venv_rel_dir)
+            assert os.path.isdir(venv_dir)
+            safe_rmtree(venv_dir)
+
         result = rule_runner.request(ProcessResult, [process])
         output_str = result.stdout.decode()
         mo = re.search(r"CWD: (.*)\n", output_str)