diff --git a/buildscripts/resmokelib/config.py b/buildscripts/resmokelib/config.py
index 693c2ac8266..1f1af9d29d8 100644
--- a/buildscripts/resmokelib/config.py
+++ b/buildscripts/resmokelib/config.py
@@ -219,6 +219,8 @@ DEFAULTS = {
     "no_hooks": False,
     # Avoids performing signature verification on test extensions at load time.
     "skip_extensions_signature_verification": False,
+    # Enable shell JS debugging
+    "shell_jsdebugmode": False,
 }
 
 _SuiteOptions = collections.namedtuple(
@@ -739,6 +741,9 @@ SHARD_INDEX = None
 # JSON containing historic test runtimes
 HISTORIC_TEST_RUNTIMES = None
 
+# Shell debug options
+SHELL_JSDEBUGMODE = None
+
 ##
 # Internally used configuration options that aren't exposed to the user
 ##
diff --git a/buildscripts/resmokelib/configure_resmoke.py b/buildscripts/resmokelib/configure_resmoke.py
index 1905229a959..a183a51d6e5 100644
--- a/buildscripts/resmokelib/configure_resmoke.py
+++ b/buildscripts/resmokelib/configure_resmoke.py
@@ -837,6 +837,8 @@ flags in common: {common_set}
     _config.NO_HOOKS = config.pop("no_hooks")
     _config.HANG_ANALYZER_HOOK_TIMEOUT = config.pop("hang_analyzer_hook_timeout")
 
+    _config.SHELL_JSDEBUGMODE = config.pop("shell_jsdebugmode")
+
     # Internal testing options.
     _config.INTERNAL_PARAMS = config.pop("internal_params")
 
diff --git a/buildscripts/resmokelib/core/programs.py b/buildscripts/resmokelib/core/programs.py
index 3f2fe58f96f..8796045e0af 100644
--- a/buildscripts/resmokelib/core/programs.py
+++ b/buildscripts/resmokelib/core/programs.py
@@ -547,6 +547,10 @@ def mongo_shell_program(
     if config.SHELL_GRPC or mongod_set_parameters.get("useGrpcForSearch"):
         args.append("--gRPC")
 
+    if config.SHELL_JSDEBUGMODE:
+        # relay to the shell flags
+        kwargs["jsDebugMode"] = ""
+
     if connection_string is not None:
         # The --host and --port options are ignored by the mongo shell when an explicit connection
         # string is specified. We remove these options to avoid any ambiguity with what server the
diff --git a/buildscripts/resmokelib/run/__init__.py b/buildscripts/resmokelib/run/__init__.py
index 62160aa4895..fed9191ad3f 100644
--- a/buildscripts/resmokelib/run/__init__.py
+++ b/buildscripts/resmokelib/run/__init__.py
@@ -1873,6 +1873,13 @@ class RunPlugin(PluginInterface):
             help="Regex to filter mocha-style tests to run.",
         )
 
+        parser.add_argument(
+            "--shellJSDebugMode",
+            dest="shell_jsdebugmode",
+            action="store_true",
+            help="Enable JavaScript debugger for spawned mongo shells.",
+        )
+
         parser.add_argument(
             "--noValidateSelectorPaths",
             dest="validate_selector_paths",
diff --git a/buildscripts/tests/resmoke_end2end/suites/resmoke_debugger_nodb.yml b/buildscripts/tests/resmoke_end2end/suites/resmoke_debugger_nodb.yml
new file mode 100644
index 00000000000..3c0ecfe2189
--- /dev/null
+++ b/buildscripts/tests/resmoke_end2end/suites/resmoke_debugger_nodb.yml
@@ -0,0 +1,10 @@
+test_kind: js_test
+
+selector:
+  roots:
+    - buildscripts/tests/resmoke_end2end/testfiles/debugger/*.js
+
+executor:
+  config:
+    shell_options:
+      nodb: ""
diff --git a/buildscripts/tests/resmoke_end2end/test_resmoke_js_debugger.py b/buildscripts/tests/resmoke_end2end/test_resmoke_js_debugger.py
new file mode 100644
index 00000000000..afbd995a61f
--- /dev/null
+++ b/buildscripts/tests/resmoke_end2end/test_resmoke_js_debugger.py
@@ -0,0 +1,300 @@
+"""Test resmoke's JavaScript debugger functionality."""
+
+import io
+import logging
+import os
+import re
+import subprocess
+import sys
+import unittest
+from shutil import rmtree
+
+import pexpect
+
+
+class _ResmokeSelftest(unittest.TestCase):
+    @classmethod
+    def setUpClass(cls):
+        cls.test_dir = os.path.normpath("/data/db/selftest")
+
+    def setUp(self):
+        self.logger = logging.getLogger(self._testMethodName)
+        self.logger.setLevel(logging.DEBUG)
+        handler = logging.StreamHandler(sys.stdout)
+        handler.setFormatter(logging.Formatter(fmt="%(message)s"))
+        self.logger.addHandler(handler)
+
+        self.logger.info("Cleaning temp directory %s", self.test_dir)
+        rmtree(self.test_dir, ignore_errors=True)
+        os.makedirs(self.test_dir, mode=0o755, exist_ok=True)
+
+
+def execute_resmoke(resmoke_args, subcommand="run"):
+    return subprocess.run(
+        [sys.executable, "buildscripts/resmoke.py", subcommand] + resmoke_args,
+        text=True,
+        stdout=subprocess.PIPE,
+        stderr=subprocess.PIPE,
+    )
+
+
+class TestJSDebugger(_ResmokeSelftest):
+    """Test suite for JavaScript debugger functionality."""
+
+    def test_debugger_without_flag(self):
+        """Test that debugger statements are no-ops when --shellJSDebugMode is not set."""
+        # Without the flag, debugger statements should be no-ops, so this test passes
+        resmoke_args = [
+            "--suites=buildscripts/tests/resmoke_end2end/suites/resmoke_debugger_nodb.yml",
+            "buildscripts/tests/resmoke_end2end/testfiles/debugger/debugger_statement.js",
+        ]
+        result = execute_resmoke(resmoke_args)
+        self.assertEqual(result.returncode, 0)
+
+    def test_debugger_waits_for_input(self):
+        """Test that debugger pauses execution when hitting a debugger statement."""
+        # This test verifies the debugger is activated by confirming it pauses execution
+        # Note: The mongo shell's debugger requires /dev/tty for interactive input,
+        # so we can only verify that it pauses, not that it responds to commands in automation
+        resmoke_cmd = [
+            sys.executable,
+            "buildscripts/resmoke.py",
+            "run",
+            f"--dbpathPrefix={self.test_dir}",
+            "--shellJSDebugMode",
+            "--suites=buildscripts/tests/resmoke_end2end/suites/resmoke_debugger_nodb.yml",
+            "buildscripts/tests/resmoke_end2end/testfiles/debugger/debugger_statement.js",
+        ]
+
+        process = subprocess.Popen(
+            resmoke_cmd,
+            stdin=subprocess.PIPE,
+            stdout=subprocess.PIPE,
+            stderr=subprocess.STDOUT,
+            text=True,
+        )
+
+        # Wait for a short time - the debugger should pause and not complete
+        try:
+            stdout, _ = process.communicate(timeout=10)
+            # If we get here without timeout, the debugger didn't activate properly
+            self.logger.error("Test output:\n%s", stdout)
+            self.fail("Expected debugger to pause execution, but test completed")
+        except subprocess.TimeoutExpired:
+            # This is the expected behavior - debugger is waiting for input
+            process.kill()
+            stdout, _ = process.communicate()
+            self.logger.info("Debugger correctly paused execution. Output:\n%s", stdout)
+            # Verify the debugger prompt appeared
+            self.assertIn("JSDEBUG>", stdout)
+            self.assertIn("paused in 'debugger' statement", stdout)
+
+
+class TestJSDebuggerInteractive(_ResmokeSelftest):
+    """Test suite for interactive JavaScript debugger functionality."""
+
+    def run_debugger_test(self, test_file, commands, timeout=30):
+        """Helper to run debugger and execute commands.
+
+        Args:
+            test_file: Path to the JS test file
+            commands: List of (command, expected_output) tuples
+            timeout: Maximum time to wait for each command
+
+        Returns:
+            Full output from the session
+        """
+        resmoke_cmd = " ".join(
+            [
+                sys.executable,
+                "buildscripts/resmoke.py",
+                "run",
+                f"--dbpathPrefix={self.test_dir}",
+                "--shellJSDebugMode",
+                "--suites=buildscripts/tests/resmoke_end2end/suites/resmoke_debugger_nodb.yml",
+                test_file,
+            ]
+        )
+
+        child = pexpect.spawn(resmoke_cmd, timeout=timeout, encoding="utf-8")
+
+        # Use StringIO to capture all output
+        output_buffer = io.StringIO()
+        child.logfile = output_buffer
+
+        try:
+            # Wait for initial debugger prompts - there are usually two in the initial pause
+            child.expect("JSDEBUG>", timeout=20)
+            self.logger.info("First debugger prompt detected")
+
+            # Wait for the "Type 'dbcont' to continue" prompt
+            child.expect("JSDEBUG>", timeout=5)
+            self.logger.info("Second debugger prompt detected, ready for commands")
+
+            # Execute each command
+            for cmd, expected in commands:
+                self.logger.info(f"Sending command: {cmd}")
+                child.sendline(cmd)
+
+                # Wait for the next prompt to ensure command completed
+                # and capture what comes before it
+                try:
+                    child.expect("JSDEBUG>", timeout=5)
+                    command_output = child.before if hasattr(child, "before") else ""
+                except pexpect.TIMEOUT:
+                    command_output = ""
+
+                # Also check what's in the full buffer
+                full_buffer = output_buffer.getvalue()
+                self.logger.info(
+                    f"Full buffer so far ({len(full_buffer)} chars, last 1000):\n{full_buffer[-1000:]}"
+                )
+
+                if expected:
+                    # Log what we're looking for and what we got back
+                    self.logger.info(f"Expect to find in output: {expected}")
+                    self.logger.info(
+                        f"child.before output (last 1000 chars): {command_output[-1000:] if command_output else 'empty'}"
+                    )
+
+                    # Check if expected is in the command output or full buffer
+                    search_text = full_buffer  # Use full buffer instead of just child.before
+                    if expected not in search_text:
+                        # Try to match as regex
+                        if not re.search(expected, search_text):
+                            self.logger.error(f"Pattern '{expected}' not found")
+                            self.logger.error(f"Full buffer:\n{full_buffer}")
+                            raise AssertionError(f"Pattern '{expected}' not found in output")
+                    self.logger.info(f"Successfully found expected pattern: {expected}")
+
+            # Wait for process to finish or timeout
+            try:
+                child.expect(pexpect.EOF, timeout=10)
+            except pexpect.TIMEOUT:
+                pass
+
+            # Return all collected output
+            full_output = output_buffer.getvalue()
+            self.logger.info(f"Full output length: {len(full_output)} chars")
+            return full_output
+
+        finally:
+            child.close(force=True)
+            output_buffer.close()
+
+    def test_debugger_continue_with_dbcont(self):
+        """Test that dbcont command continues execution."""
+        commands = [
+            ("dbcont", None),  # Continue execution
+        ]
+
+        self.run_debugger_test(
+            "buildscripts/tests/resmoke_end2end/testfiles/debugger/debugger_statement.js",
+            commands,
+        )
+
+        # If we get here without timeout, the test passed
+        pass
+
+    def test_debugger_inspect_variables(self):
+        """Test inspecting variables at debugger breakpoint."""
+        commands = [
+            # Check variable outputs
+            ("x", "42"),
+            ("y", r'[ "a", 15, [ 1, 2, 3 ] ]'),
+            ("z", r'{ "foo" : [ 3, "bar" ] }'),
+            # ("z", r'[ 3, "bar" ] }'),
+            ("dbcont", None),  # Continue
+        ]
+
+        output = self.run_debugger_test(
+            "buildscripts/tests/resmoke_end2end/testfiles/debugger/debugger_statement.js",
+            commands,
+        )
+
+        self.assertIn("42", output)
+
+    def test_debugger_undefined_variable(self):
+        """Test that accessing undefined variables shows ReferenceError."""
+        commands = [
+            ("q", "ReferenceError"),  # q is not defined
+            ("dbcont", None),
+        ]
+
+        output = self.run_debugger_test(
+            "buildscripts/tests/resmoke_end2end/testfiles/debugger/debugger_statement.js",
+            commands,
+        )
+
+        self.assertIn("ReferenceError", output)
+
+    def test_debugger_syntax_error(self):
+        """Test that syntax errors are caught in debugger."""
+        commands = [
+            ("]]", "SyntaxError"),  # Invalid syntax
+            ("dbcont", None),
+        ]
+
+        output = self.run_debugger_test(
+            "buildscripts/tests/resmoke_end2end/testfiles/debugger/debugger_statement.js",
+            commands,
+        )
+
+        self.assertIn("SyntaxError", output)
+
+    def test_debugger_assertion_error(self):
+        """Test that assertion failures are shown in debugger."""
+        commands = [
+            ("assert.eq(1, 2)", None),  # Should fail - don't expect specific text
+            ("dbcont", None),
+        ]
+
+        output = self.run_debugger_test(
+            "buildscripts/tests/resmoke_end2end/testfiles/debugger/debugger_statement.js",
+            commands,
+        )
+
+        # The assertion should fail with an error message containing relevant keywords
+        # The mongo shell may show different error formats
+        self.assertTrue(
+            ("1" in output and "2" in output)  # Numbers from assertion
+            or "Error" in output
+            or "assert" in output.lower(),
+            f"Expected assertion error output, got: {output[:500]}",
+        )
+
+    def test_debugger_modify_variables(self):
+        """Test modifying variables at debugger breakpoint."""
+        # Create a test file that expects modified variables
+        commands = [
+            ("x", "42"),  # Check original value
+            ("x = 7", None),  # Modify x
+            ("y[1]", "15"),  # Check array element
+            ("y[1] = 99", None),  # Modify array
+            ("dbcont", None),  # Continue - should pass assertions
+        ]
+
+        output = self.run_debugger_test(
+            "buildscripts/tests/resmoke_end2end/testfiles/debugger/simple_debugger.js",
+            commands,
+        )
+
+        # The test should pass because we modified the variables
+        self.assertIn("Test Passed", output)
+
+    def test_debugger_complex_expressions(self):
+        """Test evaluating complex expressions in debugger."""
+        commands = [
+            ("x + 10", "52"),  # Math expression
+            ("typeof x", "number"),  # Type check
+            ("[1,2,3].length", "3"),  # Array operations
+            ("dbcont", None),
+        ]
+
+        output = self.run_debugger_test(
+            "buildscripts/tests/resmoke_end2end/testfiles/debugger/debugger_statement.js",
+            commands,
+        )
+
+        self.assertIn("52", output)
+        self.assertIn("number", output)
diff --git a/buildscripts/tests/resmoke_end2end/testfiles/debugger/debugger_statement.js b/buildscripts/tests/resmoke_end2end/testfiles/debugger/debugger_statement.js
new file mode 100644
index 00000000000..0614ed721ea
--- /dev/null
+++ b/buildscripts/tests/resmoke_end2end/testfiles/debugger/debugger_statement.js
@@ -0,0 +1,9 @@
+let x = 42;
+let y = ["a", 15, [1, 2, 3]];
+let z = {"foo": [3, "bar"]};
+
+// should be no-op without debug mode
+debugger; // eslint-disable-line no-debugger
+
+assert.eq(x, 42);
+print("Test Passed!");
diff --git a/buildscripts/tests/resmoke_end2end/testfiles/debugger/simple_debugger.js b/buildscripts/tests/resmoke_end2end/testfiles/debugger/simple_debugger.js
new file mode 100644
index 00000000000..dad20be4c04
--- /dev/null
+++ b/buildscripts/tests/resmoke_end2end/testfiles/debugger/simple_debugger.js
@@ -0,0 +1,10 @@
+// Test that the debugger statement is hit and variables can be inspected/modified
+let x = 42;
+let y = ["a", 15, [1, 2, 3]];
+
+debugger; // eslint-disable-line no-debugger
+
+// These assertions will fail unless debugger modifies the variables
+assert.eq(x, 7);
+assert.eq(y[1], 99);
+print("Test Passed!");
diff --git a/poetry.lock b/poetry.lock
index d0d0e9a4056..672eb4b41a5 100644
--- a/poetry.lock
+++ b/poetry.lock
@@ -2829,6 +2829,22 @@ files = [
     {file = "pathspec-0.12.1.tar.gz", hash = "sha256:a482d51503a1ab33b1c67a6c3813a26953dbdc71c31dacaef9a838c4e29f5712"},
 ]
 
+[[package]]
+name = "pexpect"
+version = "4.9.0"
+description = "Pexpect allows easy control of interactive console applications."
+optional = false
+python-versions = "*"
+groups = ["testing"]
+markers = "platform_machine != \"s390x\" and platform_machine != \"ppc64le\" or platform_machine == \"s390x\" or platform_machine == \"ppc64le\""
+files = [
+    {file = "pexpect-4.9.0-py2.py3-none-any.whl", hash = "sha256:7236d1e080e4936be2dc3e326cec0af72acf9212a7e1d060210e70a47e253523"},
+    {file = "pexpect-4.9.0.tar.gz", hash = "sha256:ee7d41123f3c9911050ea2c2dac107568dc43b2d3b0c7557a33212c398ead30f"},
+]
+
+[package.dependencies]
+ptyprocess = ">=0.5"
+
 [[package]]
 name = "pipx"
 version = "1.6.0"
@@ -3059,6 +3075,19 @@ files = [
 dev = ["abi3audit", "black", "check-manifest", "coverage", "packaging", "pylint", "pyperf", "pypinfo", "pytest-cov", "requests", "rstcheck", "ruff", "sphinx", "sphinx_rtd_theme", "toml-sort", "twine", "virtualenv", "vulture", "wheel"]
 test = ["pytest", "pytest-xdist", "setuptools"]
 
+[[package]]
+name = "ptyprocess"
+version = "0.7.0"
+description = "Run a subprocess in a pseudo terminal"
+optional = false
+python-versions = "*"
+groups = ["testing"]
+markers = "platform_machine != \"s390x\" and platform_machine != \"ppc64le\" or platform_machine == \"s390x\" or platform_machine == \"ppc64le\""
+files = [
+    {file = "ptyprocess-0.7.0-py2.py3-none-any.whl", hash = "sha256:4b41f3967fce3af57cc7e94b888626c18bf37a083e3651ca8feeb66d492fef35"},
+    {file = "ptyprocess-0.7.0.tar.gz", hash = "sha256:5c5d0a3b48ceee0b48485e0c26037c0acd7d29765ca3fbb5cb3831d347423220"},
+]
+
 [[package]]
 name = "puremagic"
 version = "1.28"
@@ -5855,4 +5884,4 @@ libdeps = ["cxxfilt", "eventlet", "flask", "flask-cors", "gevent", "lxml", "prog
 [metadata]
 lock-version = "2.1"
 python-versions = ">=3.10,<4.0"
-content-hash = "e49289dec8b835ef0ea7669f80b251da77afc4d70bd6fbd8ee4d6a2b0f04677e"
+content-hash = "c4a064d90a866bf24bdc2d77d8f10147a1a6cf2d94f193e064cf8405250449cd"
diff --git a/pyproject.toml b/pyproject.toml
index b881fd54b93..adf38690c14 100644
--- a/pyproject.toml
+++ b/pyproject.toml
@@ -167,6 +167,7 @@ distro = "^1.9.0"
 dnspython = "^2.6.1"
 proxy-protocol = "^0.11.3"
 pkce = "^1.0.3"
+pexpect = "^4.9.0"
 oauthlib = "^3.1.1"
 requests-oauthlib = "^2.0.0"
 packaging = "^25.0"
diff --git a/src/mongo/shell/debugger/README.md b/src/mongo/shell/debugger/README.md
index bde54fc0d00..b47cbd83490 100644
--- a/src/mongo/shell/debugger/README.md
+++ b/src/mongo/shell/debugger/README.md
@@ -1,6 +1,8 @@
 # JS Debugging in the MongoDB Shell
 
 
+Use the `--shellJSDebugMode` flag for resmoke (or the `--jsDebugMode` flag directly on the mongo shell) to trigger an interactive debug prompt when `debugger` statements are hit in JS test code.
+
 Sample JS Test:
 ```js
 let x = 42;
@@ -66,3 +68,22 @@ Test Passed!
 All pids dead / alive (0): 
 Searching for files in: /home/ubuntu/mongo
 ```
+
+## Resmoke
+
+Use the `--shellJSDebugMode` flag in resmoke to stop on debugger statements:
+```bash
+buildscripts/resmoke.py run --suites=no_passthrough --shellJSDebugMode jstests/my_test.js
+```
+
+Update variables `x` and `q` to repair the failing assertions:
+```
+JSDEBUG> JavaScript execution paused in 'debugger' statement.
+JSDEBUG> Type 'dbcont' to continue
+JSDEBUG@jstests/my_test.js:5> x = 7
+7
+JSDEBUG@jstests/my_test.js:5> q = "foo"
+foo
+JSDEBUG@jstests/my_test.js:5> dbcont
+[js_test:my_test] Test Passed!
+```