diff --git a/conda_build/_rattler_build/compat.py b/conda_build/_rattler_build/compat.py
index 0bf85dd187..3ead49e3c2 100644
--- a/conda_build/_rattler_build/compat.py
+++ b/conda_build/_rattler_build/compat.py
@@ -2,6 +2,9 @@
 # SPDX-License-Identifier: BSD-3-Clause
 from __future__ import annotations
 
+import os
+import sys
+import time
 from dataclasses import dataclass, field
 from pathlib import Path
 from typing import TYPE_CHECKING
@@ -13,16 +16,17 @@
     RattlerBuildError,
     RecipeParseError,
 )
+from rattler_build.debug import DebugSession
 from rattler_build.progress import SimpleProgressCallback
 from rattler_build.render import RenderConfig
-from rattler_build.stage0 import Stage0Recipe
+from rattler_build.stage0 import MultiOutputRecipe, Stage0Recipe
 from rattler_build.tool_config import PlatformConfig, ToolConfiguration
 from rattler_build.variant_config import VariantConfig
 
 from ..build import handle_anaconda_upload
 from ..config import CondaPkgFormat
 from ..exceptions import CondaBuildUserError
-from ..utils import get_logger
+from ..utils import get_logger, on_win
 
 if TYPE_CHECKING:
     import argparse
@@ -48,6 +52,7 @@ class RecipeResult:
     recipe_path: str
     outputs: list[OutputResult] = field(default_factory=list)
     error: str | None = None
+    activation_string: str | None = None
 
     @property
     def failed(self) -> bool:
@@ -125,6 +130,15 @@ def check_arguments_rattler(
             "channel",
             "override_channels",
         },
+        "debug": {
+            "recipe",
+            "output_id",
+            "variant_config_files",
+            "exclusive_config_files",
+            "channel",
+            "override_channels",
+            "activate_string_only",
+        },
     }
 
     # check for unsupported CLI arguments
@@ -198,6 +212,62 @@ def process_recipe(
             print(yaml.safe_dump(data, indent=2, sort_keys=False))
         return result
 
+    if command == "debug":
+        if isinstance(recipe, MultiOutputRecipe):
+            if not list(rendered):
+                sys.exit(
+                    f"No rendered outputs were produced for {Path(recipe_path).resolve()}"
+                )
+            if parsed_args.output_id is None:
+                output_names = sorted(
+                    {
+                        variant.recipe.to_dict().get("package", {}).get("name")
+                        for variant in rendered
+                    }
+                )
+                raise CondaBuildUserError(
+                    f"\nFound {len(output_names)} outputs in recipe. Please specify one "
+                    f"using --output-id. Available outputs: {', '.join(output_names)}"
+                )
+            else:
+                selected_output = None
+                for variant in rendered:
+                    name = variant.recipe.to_dict().get("package", {}).get("name")
+                    if name == parsed_args.output_id:
+                        selected_output = variant
+                        break
+
+                if selected_output is None:
+                    raise CondaBuildUserError(
+                        f"Output '{parsed_args.output_id}' not found. "
+                    )
+
+        else:
+            selected_output = rendered[0]
+        try:
+            session = DebugSession.create(
+                variant=selected_output,
+                tool_config=tool_config,
+                output_dir=os.path.join(output_dir, f"debug_{int(time.time() * 1000)}"),
+                channels=channels,
+                progress_callback=CondaProgressCallback(show_logs=True),
+            )
+        except RattlerBuildError as e:
+            result.error = (
+                f"Failed to setup debug scripts for output {selected_output}: {e}"
+            )
+            return result
+
+        result.activation_string = (
+            "cd {work_dir} && {source} {activation_file}\n".format(
+                work_dir=session.paths.work_dir,
+                source="call" if on_win else "source",
+                activation_file=session.paths.build_env_script,
+            )
+        )
+
+        return result
+
     for i, variant in enumerate(rendered, 1):
         print(
             f"\nBuilding variant {i}/{len(rendered)} for recipe {Path(recipe_path).resolve()}"
@@ -291,9 +361,11 @@ def process_recipe(
     return result
 
 
-def run_rattler(command: str, parsed_args: argparse.Namespace, config: Config) -> int:
+def run_rattler(
+    command: str, parsed_args: argparse.Namespace, config: Config
+) -> str | int:
     """Run rattler-build for v1 recipes"""
-    if command not in ("build", "render"):
+    if command not in ("build", "debug", "render"):
         raise ValueError(f"Unrecognized subcommand: {command}")
 
     # Initialize configuration defaults
@@ -416,7 +488,7 @@ def get_config_value(name):
         else:
             package_format = ".tar.bz2"
 
-    if command == "render":
+    if command in ("debug", "render"):
         recipes = [str(Path(parsed_args.recipe) / "recipe.yaml")]
     else:
         recipes = [
@@ -444,27 +516,48 @@ def get_config_value(name):
             )
         )
 
-    if command == "render":
-        failed = [r for r in recipe_results if r.failed]
-        if failed:
-            msg = "\n".join(
-                [
-                    "Recipe render failures:",
-                    *[
-                        f"  - {Path(r.recipe_path).resolve()}: {r.error or 'Unknown error'}"
-                        for r in failed
-                    ],
-                ]
-            )
-            raise CondaBuildUserError(msg)
-        return 0
+        if command == "render":
+            # we are expecting a single recipe result
+            result = recipe_results[0]
+            if result.failed:
+                recipe_path = Path(result.recipe_path).resolve()
+
+                raise CondaBuildUserError(
+                    "\n".join(
+                        [
+                            "Error:   × Failed to render recipe",
+                            f"  ╰─▶ {recipe_path}",
+                            "",
+                            f"      {result.error}",
+                        ]
+                    )
+                )
+            return 0
+
+        if command == "debug":
+            # we are expecting a single recipe result
+            result = recipe_results[0]
+            if result.failed:
+                recipe_path = Path(result.recipe_path).resolve()
+
+                raise CondaBuildUserError(
+                    "\n".join(
+                        [
+                            "Error:   Failed to debug recipe",
+                            f"  ╰─▶ {recipe_path}",
+                            "",
+                            f"      {result.error}",
+                        ]
+                    )
+                )
+            return result.activation_string
 
-    recipe_count = len(recipe_results)
-    total_outputs = sum(len(r.outputs) for r in recipe_results)
-    succeeded_outputs = sum(
-        1 for r in recipe_results for output in r.outputs if output.success
-    )
-    failed_outputs = total_outputs - succeeded_outputs
+        recipe_count = len(recipe_results)
+        total_outputs = sum(len(r.outputs) for r in recipe_results)
+        succeeded_outputs = sum(
+            1 for r in recipe_results for output in r.outputs if output.success
+        )
+        failed_outputs = total_outputs - succeeded_outputs
 
     print("\n=== Build summary ===")
     print(
diff --git a/conda_build/api.py b/conda_build/api.py
index fb8555c07c..083ef16b3f 100644
--- a/conda_build/api.py
+++ b/conda_build/api.py
@@ -40,6 +40,34 @@
     StatsDict = dict[str, Any]
 
 
+def _error_if_package_contains_recipe_yaml(pkg_path: str) -> None:
+    from contextlib import redirect_stdout
+    from io import StringIO
+
+    import conda_package_handling.api
+
+    buffer = StringIO()
+    with redirect_stdout(buffer):
+        conda_package_handling.api.list_contents(
+            pkg_path,
+            components=["info"],
+        )
+
+    pkg_contents = [
+        line.strip() for line in buffer.getvalue().splitlines() if line.strip()
+    ]
+
+    for recipe_yaml_file in (
+        "info/recipe/recipe.yaml",
+        "info/recipe/rendered_recipe.yaml",
+    ):
+        if recipe_yaml_file in pkg_contents:
+            raise ValueError(
+                f"Package '{pkg_path}' contains v1 '{recipe_yaml_file.rsplit('/', 1)[-1]}' file, "
+                "which is currently not supported by conda debug."
+            )
+
+
 def render(
     recipe_path: str | os.PathLike | Path,
     config: Config | None = None,
@@ -659,6 +687,9 @@ def debug(
             )
         else:
             test_input = recipe_or_package_path_or_metadata_tuples
+
+        _error_if_package_contains_recipe_yaml(test_input)
+
         # use the package to create an env and extract the test files.  Stop short of running the tests.
         # tell people what steps to take next
         with log_context:
diff --git a/conda_build/cli/main_debug.py b/conda_build/cli/main_debug.py
index 2cc18fc51a..9cc0a876d8 100644
--- a/conda_build/cli/main_debug.py
+++ b/conda_build/cli/main_debug.py
@@ -4,12 +4,15 @@
 
 import logging
 import sys
+from pathlib import Path
 from typing import TYPE_CHECKING
 
 from conda.base.context import context
 
 from .. import api
-from ..utils import on_win
+from .._rattler_build.compat import check_arguments_rattler, run_rattler
+from ..config import get_or_merge_config
+from ..utils import is_v1_recipe, on_win
 from . import validators as valid
 from .main_render import get_render_parser
 
@@ -98,12 +101,29 @@ def execute(args: Sequence[str] | None = None) -> int:
     parsed = parser.parse_args(args)
     context.__init__(argparse_args=parsed)
 
-    try:
-        activation_string = api.debug(
-            parsed.recipe_or_package_file_path,
-            verbose=(not parsed.activate_string_only),
-            **parsed.__dict__,
+    # mixed recipe formats found, error out
+    if (Path(parsed.recipe_or_package_file_path) / "recipe.yaml").is_file() and (
+        Path(parsed.recipe_or_package_file_path) / "meta.yaml"
+    ).is_file():
+        print(
+            "Cannot process several recipe versions at the same time!", file=sys.stderr
         )
+        return 1
+
+    try:
+        if is_v1_recipe(parsed.recipe_or_package_file_path):
+            config = get_or_merge_config(None, **parsed.__dict__)
+            parsed_only_recipe = parser.parse_args([parsed.recipe_or_package_file_path])
+            check_arguments_rattler(parser.prog.split()[-1], parsed, parsed_only_recipe)
+            parsed.recipe = parsed.recipe_or_package_file_path
+            command = parser.prog.split()[-1]
+            activation_string = run_rattler(command, parsed, config)
+        else:
+            activation_string = api.debug(
+                parsed.recipe_or_package_file_path,
+                verbose=(not parsed.activate_string_only),
+                **parsed.__dict__,
+            )
 
         if not parsed.activate_string_only:
             print("#" * 80)
@@ -113,7 +133,11 @@ def execute(args: Sequence[str] | None = None) -> int:
 
         print(activation_string)
         if not parsed.activate_string_only:
-            test_file = "conda_test_runner.bat" if on_win else "conda_test_runner.sh"
+            test_file = (
+                f"conda_{'build' if is_v1_recipe(parsed.recipe_or_package_file_path) else 'test_runner'}."
+                f"{'bat' if on_win else 'sh'}"
+            )
+
             print(
                 f"To run your tests, you might want to start with running the {test_file} file."
             )
diff --git a/conda_build/render.py b/conda_build/render.py
index c78100d238..062b63a7cd 100644
--- a/conda_build/render.py
+++ b/conda_build/render.py
@@ -67,7 +67,7 @@
 
 from . import environ, exceptions, source, utils
 from .config import CondaPkgFormat
-from .exceptions import CondaBuildUserError, DependencyNeedsBuildingError
+from .exceptions import CondaBuildUserError, DependencyNeedsBuildingError, RecipeError
 from .index import get_build_index
 from .metadata import MetaData, MetaDataTuple, combine_top_level_metadata_with_output
 from .utils import (
@@ -1082,6 +1082,8 @@ def render_recipe(
             m = MetaData(str(recipe), config=config)
         except exceptions.YamlParsingError as e:
             sys.exit(e.error_msg())
+        except OSError as e:
+            raise RecipeError(str(e)) from e
 
         # important: set build id *before* downloading source.  Otherwise source goes into a different
         #    build folder.
diff --git a/docs/source/user-guide/v1-recipes.rst b/docs/source/user-guide/v1-recipes.rst
index a1f5aef84e..8dcb7a0303 100644
--- a/docs/source/user-guide/v1-recipes.rst
+++ b/docs/source/user-guide/v1-recipes.rst
@@ -9,8 +9,8 @@ To get started with building v1 recipes, simply invoke ``conda-build`` and pass
 the recipe's directory. ``conda-build`` will recognize the recipe format and
 handle the build through ``py-rattler-build``.
 
-``conda-build`` currently supports v1 recipes in the ``conda build`` and
-``conda render`` commands.
+``conda-build`` currently supports v1 recipes in the ``conda build``,
+``conda render`` and ``conda-debug`` commands.
 
 Build configuration is done in the same way as for v0 recipes. Many configuration settings are translated into rattler-build equivalents and
 passed to ``py-rattler-build``. The following ``conda-build`` command-line arguments (and their corresponding settings in ``~/.condarc`` file) are
@@ -48,6 +48,17 @@ supported:
 - ``--recipe``
 - ``--variant-config-files``
 
+``conda debug``
+================
+
+- ``--activate-string-only``
+- ``--channel``
+- ``--exclusive-config-file``
+- ``--output-id``
+- ``--override-channels``
+- ``--recipe``
+- ``--variant-config-files``
+
 Package upload
 ==============
 
@@ -88,7 +99,6 @@ For example, to authenticate with a private channel hosted on ``prefix.dev``:
 After this setup, ``conda-build`` will be able to access packages hosted on the
 private channel.
 
-
 Limitations
 ===========
 
diff --git a/news/5950-conda-debug-v1.md b/news/5950-conda-debug-v1.md
new file mode 100644
index 0000000000..71bcb38a55
--- /dev/null
+++ b/news/5950-conda-debug-v1.md
@@ -0,0 +1,19 @@
+### Enhancements
+
+* Add support for v1 recipes to `conda-debug` (#5950).
+
+### Bug fixes
+
+* <news item>
+
+### Deprecations
+
+* <news item>
+
+### Docs
+
+* Add `conda-debug` command to v1 recipe docs. (#5950)
+
+### Other
+
+* <news item>
diff --git a/recipe/meta.yaml b/recipe/meta.yaml
index 966b2e63cf..71ed91e573 100644
--- a/recipe/meta.yaml
+++ b/recipe/meta.yaml
@@ -50,7 +50,7 @@ requirements:
     - pkginfo
     - psutil
     - py-lief
-    - py-rattler-build >=0.61.4
+    - py-rattler-build >=0.65.1
     - python
     - python-libarchive-c
     - pyyaml
diff --git a/tests/cli/test_main_debug.py b/tests/cli/test_main_debug.py
index ae4f22441d..0395536ad9 100644
--- a/tests/cli/test_main_debug.py
+++ b/tests/cli/test_main_debug.py
@@ -1,5 +1,6 @@
 # Copyright (C) 2014 Anaconda, Inc
 # SPDX-License-Identifier: BSD-3-Clause
+import os
 import sys
 from pathlib import Path
 from unittest import mock
@@ -7,8 +8,13 @@
 import pytest
 from pytest import CaptureFixture, MonkeyPatch
 
+from conda_build.cli import main_build as build
 from conda_build.cli import main_debug as debug
 from conda_build.cli import validators as valid
+from conda_build.exceptions import CondaBuildUserError
+from conda_build.utils import on_win
+
+from ..utils import metadata_dir
 
 
 def test_main_debug_help_message(capsys: CaptureFixture, monkeypatch: MonkeyPatch):
@@ -51,3 +57,80 @@ def test_main_debug_happy_path(
         assert captured.err == ""
 
         assert len(mock_debug.mock_calls) == 2
+
+
+def test_debug_v1_recipe(testing_workdir, capsys: CaptureFixture):
+    """
+    Test conda-debug functionality for v1 recipe. The test uses a multi-output recipe.
+    """
+    recipe_dir = os.path.join(
+        metadata_dir, "..", "variants", "33_v1_recipe_multi_output"
+    )
+
+    # Make sure that it fails with the expected message if output is not specified
+    args = [recipe_dir]
+    with pytest.raises(
+        CondaBuildUserError,
+        match=r"Found 2 outputs in recipe. Please specify one using --output-id.",
+    ):
+        debug.execute(args)
+
+    # Setup scripts for the first output
+    args = [recipe_dir, "--output-id", "myproject-lib"]
+    assert debug.execute(args) == 0
+
+    captured = capsys.readouterr()
+    output = captured.out
+    assert "Test environment created for debugging." in output
+    assert "rattler-build_myproject-lib" in output
+    expected = (
+        "To run your tests, you might want to start with running the conda_build.bat file."
+        if on_win
+        else "To run your tests, you might want to start with running the conda_build.sh file."
+    )
+    assert expected in output
+
+    # Setup scripts for the second output
+    # Build the recipe because second output depends on the first one
+    args = [recipe_dir, "--output-folder", testing_workdir]
+    build.execute(args)
+
+    args = [recipe_dir, "--output-id", "myproject-tools", "-c", testing_workdir]
+    assert debug.execute(args) == 0
+
+    captured = capsys.readouterr()
+    output = captured.out
+    assert "Test environment created for debugging." in output
+    assert "rattler-build_myproject-tools" in output
+    assert expected in output
+
+
+def test_error_if_package_contains_recipe_yaml(tmp_path: Path, capsys: CaptureFixture):
+    recipe_dir = Path(metadata_dir, "..", "variants", "32_v1_recipe")
+    out = tmp_path / "out"
+
+    args = [
+        str(recipe_dir),
+        "-c",
+        "conda-forge",
+        "--no-test",
+        "--output-folder",
+        str(out),
+    ]
+    build.execute(args)
+
+    pkg_files = list((out / "noarch").glob("pytest*.conda"))
+    assert len(pkg_files) == 1, pkg_files
+    pkg_file = pkg_files[0]
+
+    with pytest.raises(SystemExit) as exc:
+        debug.execute([str(pkg_file)])
+
+    assert exc.value.code == 1
+
+    captured = capsys.readouterr()
+    output = captured.out + captured.err
+    assert (
+        "contains v1 'recipe.yaml' file, which is currently not supported by conda debug."
+        in output
+    )
diff --git a/tests/requirements.txt b/tests/requirements.txt
index 5d00681860..160c88249a 100644
--- a/tests/requirements.txt
+++ b/tests/requirements.txt
@@ -17,7 +17,7 @@ pip
 pkginfo
 psutil
 py-lief
-py-rattler-build >=0.61.4 # v1 recipe support
+py-rattler-build >=0.65.1 # v1 recipe support
 pytest-rerunfailures  # for handling flaky tests
 python >=3.10
 python-libarchive-c