diff --git a/task-sdk/src/airflow/sdk/execution_time/supervisor.py b/task-sdk/src/airflow/sdk/execution_time/supervisor.py
index efc74506b62d4..a7787f1875a87 100644
--- a/task-sdk/src/airflow/sdk/execution_time/supervisor.py
+++ b/task-sdk/src/airflow/sdk/execution_time/supervisor.py
@@ -43,6 +43,7 @@
     TextIO,
     cast,
 )
+from urllib.parse import urlparse
 from uuid import UUID
 
 import attrs
@@ -1639,12 +1640,42 @@ def supervise(
     :param subprocess_logs_to_stdout: Should task logs also be sent to stdout via the main logger.
     :param client: Optional preconfigured client for communication with the server (Mostly for tests).
     :return: Exit code of the process.
+    :raises ValueError: If server URL is empty or invalid.
     """
     # One or the other
     from airflow.sdk.execution_time.secrets_masker import reset_secrets_masker
 
-    if not client and ((not server) ^ dry_run):
-        raise ValueError(f"Can only specify one of {server=} or {dry_run=}")
+    if not client:
+        if dry_run and server:
+            raise ValueError(f"Can only specify one of {server=} or {dry_run=}")
+
+        if not dry_run:
+            if not server:
+                raise ValueError(
+                    "Invalid execution API server URL. Please ensure that a valid URL is configured."
+                )
+
+            try:
+                parsed_url = urlparse(server)
+            except Exception as e:
+                raise ValueError(
+                    f"Invalid execution API server URL '{server}': {e}. "
+                    "Please ensure that a valid URL is configured."
+                ) from e
+
+            if parsed_url.scheme not in ("http", "https"):
+                raise ValueError(
+                    f"Invalid execution API server URL '{server}': "
+                    "URL must use http:// or https:// scheme. "
+                    "Please ensure that a valid URL is configured."
+                )
+
+            if not parsed_url.netloc:
+                raise ValueError(
+                    f"Invalid execution API server URL '{server}': "
+                    "URL must include a valid host. "
+                    "Please ensure that a valid URL is configured."
+                )
 
     if not dag_rel_path:
         raise ValueError("dag_path is required")
diff --git a/task-sdk/tests/conftest.py b/task-sdk/tests/conftest.py
index 80c71f41a8fe8..d1866f523919c 100644
--- a/task-sdk/tests/conftest.py
+++ b/task-sdk/tests/conftest.py
@@ -20,6 +20,7 @@
 import os
 from pathlib import Path
 from typing import TYPE_CHECKING, Any, NoReturn, Protocol
+from unittest.mock import patch
 
 import pytest
 
@@ -271,3 +272,12 @@ def _make_context_dict(
         return context.model_dump(exclude_unset=True, mode="json")
 
     return _make_context_dict
+
+
+@pytest.fixture
+def patched_secrets_masker():
+    from airflow.sdk.execution_time.secrets_masker import SecretsMasker
+
+    secrets_masker = SecretsMasker()
+    with patch("airflow.sdk.execution_time.secrets_masker._secrets_masker", return_value=secrets_masker):
+        yield secrets_masker
diff --git a/task-sdk/tests/task_sdk/execution_time/test_supervisor.py b/task-sdk/tests/task_sdk/execution_time/test_supervisor.py
index 697581326706e..27b655a323db2 100644
--- a/task-sdk/tests/task_sdk/execution_time/test_supervisor.py
+++ b/task-sdk/tests/task_sdk/execution_time/test_supervisor.py
@@ -27,6 +27,7 @@
 import socket
 import sys
 import time
+from contextlib import nullcontext
 from operator import attrgetter
 from random import randint
 from time import sleep
@@ -147,6 +148,58 @@ def client_with_ti_start(make_ti_context):
     return client
 
 
+@pytest.mark.usefixtures("disable_capturing")
+class TestSupervisor:
+    @pytest.mark.parametrize(
+        "server, dry_run, expectation",
+        [
+            ("/execution/", False, pytest.raises(ValueError, match="Invalid execution API server URL")),
+            ("", False, pytest.raises(ValueError, match="Invalid execution API server URL")),
+            ("http://localhost:8080", True, pytest.raises(ValueError, match="Can only specify one of")),
+            (None, True, nullcontext()),
+            ("http://localhost:8080/execution/", False, nullcontext()),
+            ("https://localhost:8080/execution/", False, nullcontext()),
+        ],
+    )
+    def test_supervise(
+        self,
+        patched_secrets_masker,
+        server,
+        dry_run,
+        expectation,
+        test_dags_dir,
+        client_with_ti_start,
+    ):
+        """
+        Test that the supervisor validates server URL and dry_run parameter combinations correctly.
+        """
+        ti = TaskInstance(
+            id=uuid7(),
+            task_id="async",
+            dag_id="super_basic_deferred_run",
+            run_id="d",
+            try_number=1,
+            dag_version_id=uuid7(),
+        )
+
+        bundle_info = BundleInfo(name="my-bundle", version=None)
+
+        kw = {
+            "ti": ti,
+            "dag_rel_path": "super_basic_deferred_run.py",
+            "token": "",
+            "bundle_info": bundle_info,
+            "dry_run": dry_run,
+            "server": server,
+        }
+        if isinstance(expectation, nullcontext):
+            kw["client"] = client_with_ti_start
+
+        with patch.dict(os.environ, local_dag_bundle_cfg(test_dags_dir, bundle_info.name)):
+            with expectation:
+                supervise(**kw)
+
+
 @pytest.mark.usefixtures("disable_capturing")
 class TestWatchedSubprocess:
     @pytest.fixture(autouse=True)