diff --git a/docs/syntax/optional.md b/docs/syntax/optional.md
index ae054b51..efe0e759 100644
--- a/docs/syntax/optional.md
+++ b/docs/syntax/optional.md
@@ -64,6 +64,8 @@ Adding `"smartquotes"` to `myst_enable_extensions` (in the {{ confpy }}) will au
 - `'single quotes'`: 'single quotes'
 - `"double quotes"`: "double quotes"
 
+Quote characters follow the configured document language (such as Sphinx's `language` option or Docutils' `--language`, `--smart-quotes`, and `--smartquote-locales` settings), falling back to English typographic quotes when unsupported.
+
 Adding `"replacements"` to `myst_enable_extensions` (in the {{ confpy }}) will automatically convert some common typographic texts:
 
 text  | converted
diff --git a/myst_parser/parsers/docutils_.py b/myst_parser/parsers/docutils_.py
index 91ae74e3..a89c8868 100644
--- a/myst_parser/parsers/docutils_.py
+++ b/myst_parser/parsers/docutils_.py
@@ -32,7 +32,11 @@
     SortFootnotes,
     UnreferencedFootnotesDetector,
 )
-from myst_parser.parsers.mdit import create_md_parser, linkify_available
+from myst_parser.parsers.mdit import (
+    create_md_parser,
+    document_smartquotes,
+    linkify_available,
+)
 from myst_parser.warnings_ import MystWarnings, create_warning
 
 
@@ -329,7 +333,12 @@ def parse(self, inputstring: str, document: nodes.document) -> None:
                 config = merge_file_level(config, topmatter, warning)
 
         # parse content
-        parser = create_md_parser(config, DocutilsRenderer)
+        quotes = (
+            document_smartquotes(document)
+            if "smartquotes" in config.enable_extensions
+            else None
+        )
+        parser = create_md_parser(config, DocutilsRenderer, quotes=quotes)
         parser.options["document"] = document
         parser.render(inputstring)
 
diff --git a/myst_parser/parsers/mdit.py b/myst_parser/parsers/mdit.py
index b248096b..0cc124e0 100644
--- a/myst_parser/parsers/mdit.py
+++ b/myst_parser/parsers/mdit.py
@@ -4,7 +4,8 @@
 
 from __future__ import annotations
 
-from collections.abc import Callable
+from collections.abc import Callable, Iterable, Sequence
+from typing import TYPE_CHECKING
 
 from markdown_it import MarkdownIt
 from markdown_it.renderer import RendererProtocol
@@ -26,6 +27,90 @@
 
 from myst_parser.config.main import MdParserConfig
 
+if TYPE_CHECKING:
+    from docutils import nodes
+
+DEFAULT_SMARTQUOTES: tuple[str, str, str, str] = (
+    "\u201c",
+    "\u201d",
+    "\u2018",
+    "\u2019",
+)
+
+
+def _coerce_quotes(quotes: Sequence[str]) -> tuple[str, str, str, str] | None:
+    """Validate and normalize a 4-item quote sequence into a 4-tuple of strings."""
+    if len(quotes) != 4:
+        return None
+    return (quotes[0], quotes[1], quotes[2], quotes[3])
+
+
+def resolve_smartquotes(
+    language_code: str | None = None,
+    *,
+    smart_quotes: bool | str = False,
+    smartquotes_locales: Iterable[tuple[str, Sequence[str]]] | None = None,
+) -> tuple[str, str, str, str]:
+    """Resolve localized smart quote characters for ``markdown-it-py``.
+
+    Follows Docutils' ``SmartQuotes`` locale lookup (``smartchars.quotes``,
+    ``smartquotes_locales``, ``smart_quotes="alt"``, and BCP 47 subtag fallback
+    via ``normalize_language_tag``) without mutating global Docutils state.
+    Falls back to ``DEFAULT_SMARTQUOTES`` when ``language_code`` is unset or
+    has no matching quote definition.
+
+    :param language_code: Document language tag (e.g. ``"fr"``, ``"de_DE"``).
+    :param smart_quotes: Docutils ``smart_quotes`` setting; strings starting
+        with ``"alt"`` select the ``-x-altquot`` variant.
+    :param smartquotes_locales: Optional ``(language_tag, quotes)`` overrides
+        from Docutils' ``smartquotes_locales`` setting.
+    :return: A 4-tuple ``(open_double, close_double, open_single, close_single)``.
+    """
+    if not language_code or not language_code.strip():
+        return DEFAULT_SMARTQUOTES
+
+    from docutils.utils import normalize_language_tag
+    from docutils.utils.smartquotes import smartchars
+
+    quotes_map: dict[str, Sequence[str]] = dict(smartchars.quotes)
+    if smartquotes_locales:
+        for locale_tag, locale_quotes in smartquotes_locales:
+            coerced = _coerce_quotes(locale_quotes)
+            if coerced is None or not locale_tag:
+                continue
+            normalized = normalize_language_tag(locale_tag)
+            if normalized and normalized[0]:
+                quotes_map[normalized[0]] = coerced
+
+    lang = language_code.strip()
+    if isinstance(smart_quotes, str) and smart_quotes.startswith("alt"):
+        if "-x-altquot" in lang:
+            lang = lang.replace("-x-altquot", "")
+        else:
+            lang = f"{lang}-x-altquot"
+
+    for tag in normalize_language_tag(lang):
+        if tag in quotes_map:
+            coerced = _coerce_quotes(quotes_map[tag])
+            if coerced is not None:
+                return coerced
+
+    return DEFAULT_SMARTQUOTES
+
+
+def document_smartquotes(document: nodes.document, /) -> tuple[str, str, str, str]:
+    """Resolve localized smart quote characters from a Docutils document.
+
+    :param document: The Docutils document whose runtime settings are read.
+    :return: A 4-tuple ``(open_double, close_double, open_single, close_single)``.
+    """
+    settings = document.settings
+    return resolve_smartquotes(
+        getattr(settings, "language_code", None),
+        smart_quotes=getattr(settings, "smart_quotes", False),
+        smartquotes_locales=getattr(settings, "smartquotes_locales", None),
+    )
+
 
 def linkify_available() -> bool:
     """Return whether the optional ``linkify-it-py`` dependency is installed."""
@@ -36,9 +121,20 @@ def linkify_available() -> bool:
 
 
 def create_md_parser(
-    config: MdParserConfig, renderer: Callable[[MarkdownIt], RendererProtocol]
+    config: MdParserConfig,
+    renderer: Callable[[MarkdownIt], RendererProtocol],
+    *,
+    quotes: Sequence[str] | None = None,
 ) -> MarkdownIt:
-    """Return a Markdown parser with the required MyST configuration."""
+    """Return a Markdown parser with the required MyST configuration.
+
+    :param config: The MyST parser configuration.
+    :param renderer: Renderer factory passed to ``MarkdownIt``.
+    :param quotes: Optional 4-item sequence ``(open_double, close_double,
+        open_single, close_single)`` overriding ``markdown-it-py``'s default
+        typographic quote characters when ``smartquotes`` is enabled.
+    :return: Configured ``MarkdownIt`` parser instance.
+    """
 
     if config.commonmark_only:
         # see https://spec.commonmark.org/
@@ -73,6 +169,11 @@ def create_md_parser(
     if "smartquotes" in config.enable_extensions:
         md.enable("smartquotes")
         typographer = True
+        if quotes is not None:
+            coerced_quotes = _coerce_quotes(quotes)
+            if coerced_quotes is None:
+                raise ValueError("`quotes` must contain exactly 4 quote strings.")
+            md.options["quotes"] = coerced_quotes
     if "replacements" in config.enable_extensions:
         md.enable("replacements")
         typographer = True
diff --git a/myst_parser/parsers/sphinx_.py b/myst_parser/parsers/sphinx_.py
index b2a83e41..17d00add 100644
--- a/myst_parser/parsers/sphinx_.py
+++ b/myst_parser/parsers/sphinx_.py
@@ -22,7 +22,7 @@
     ResolveSectionRefs,
     SortFootnotes,
 )
-from myst_parser.parsers.mdit import create_md_parser
+from myst_parser.parsers.mdit import create_md_parser, document_smartquotes
 from myst_parser.warnings_ import create_warning
 
 SPHINX_LOGGER = logging.getLogger(__name__)
@@ -84,6 +84,11 @@ def parse(self, inputstring: str, document: nodes.document) -> None:
                 )
                 config = merge_file_level(config, topmatter, warning)
 
-        parser = create_md_parser(config, SphinxRenderer)
+        quotes = (
+            document_smartquotes(document)
+            if "smartquotes" in config.enable_extensions
+            else None
+        )
+        parser = create_md_parser(config, SphinxRenderer, quotes=quotes)
         parser.options["document"] = document
         parser.render(inputstring)
diff --git a/tests/test_docutils.py b/tests/test_docutils.py
index cabb2c03..63c7140e 100644
--- a/tests/test_docutils.py
+++ b/tests/test_docutils.py
@@ -28,7 +28,11 @@
     cli_xml,
     to_html5_demo,
 )
-from myst_parser.parsers.mdit import create_md_parser
+from myst_parser.parsers.mdit import (
+    DEFAULT_SMARTQUOTES,
+    create_md_parser,
+    resolve_smartquotes,
+)
 
 
 def test_attr_to_optparse_option():
@@ -1218,3 +1222,149 @@ def test_math_inline_double_latex_no_blank_lines():
     )
     assert "\\begin{align*}" in output
     assert_no_blank_line_in_math_env(output)
+
+
+@pytest.mark.parametrize(
+    ("language_code", "smart_quotes", "locales", "expected"),
+    [
+        pytest.param(None, False, None, DEFAULT_SMARTQUOTES, id="unset"),
+        pytest.param("", False, None, DEFAULT_SMARTQUOTES, id="empty"),
+        pytest.param("   ", False, None, DEFAULT_SMARTQUOTES, id="whitespace"),
+        pytest.param("en", False, None, DEFAULT_SMARTQUOTES, id="english"),
+        pytest.param(
+            "fr",
+            False,
+            None,
+            ("\u00ab\u00a0", "\u00a0\u00bb", "\u201c", "\u201d"),
+            id="french",
+        ),
+        pytest.param(
+            "fr",
+            "alt",
+            None,
+            ("\u00ab\u202f", "\u202f\u00bb", "\u201c", "\u201d"),
+            id="french-alt",
+        ),
+        pytest.param(
+            "fr-x-altquot",
+            "alt",
+            None,
+            ("\u00ab\u00a0", "\u00a0\u00bb", "\u201c", "\u201d"),
+            id="french-alt-toggle",
+        ),
+        pytest.param(
+            "fr_CH",
+            False,
+            None,
+            ("\u00ab", "\u00bb", "\u2039", "\u203a"),
+            id="swiss-french",
+        ),
+        pytest.param(
+            "de_AT",
+            False,
+            None,
+            ("\u201e", "\u201c", "\u201a", "\u2018"),
+            id="austrian-german-fallback",
+        ),
+        pytest.param(
+            "zh_TW",
+            False,
+            None,
+            ("\u300c", "\u300d", "\u300e", "\u300f"),
+            id="traditional-chinese",
+        ),
+        pytest.param(
+            "tlh",
+            False,
+            None,
+            DEFAULT_SMARTQUOTES,
+            id="unsupported-fallback",
+        ),
+        pytest.param(
+            "fr_FR",
+            False,
+            [("fr_FR", ("<<", ">>", "<", ">")), ("", "abcd"), ("de", "bad")],
+            ("<<", ">>", "<", ">"),
+            id="custom-locale-override",
+        ),
+    ],
+)
+def test_resolve_smartquotes(language_code, smart_quotes, locales, expected):
+    """``resolve_smartquotes`` honors Docutils locale rules without mutating globals (#806)."""
+    from docutils.utils.smartquotes import smartchars
+
+    snapshot = dict(smartchars.quotes)
+    assert (
+        resolve_smartquotes(
+            language_code,
+            smart_quotes=smart_quotes,
+            smartquotes_locales=locales,
+        )
+        == expected
+    )
+    assert smartchars.quotes == snapshot
+
+
+def test_create_md_parser_invalid_quotes():
+    """``create_md_parser`` rejects quote overrides that do not specify 4 entries."""
+    with pytest.raises(ValueError, match="exactly 4 quote strings"):
+        create_md_parser(
+            MdParserConfig(enable_extensions={"smartquotes"}),
+            DocutilsRenderer,
+            quotes=("<<", ">>"),
+        )
+
+
+@pytest.mark.parametrize(
+    ("source", "settings", "expected"),
+    [
+        pytest.param(
+            'Test\'s "double" and \'single\' and "*emph*"',
+            {
+                "language_code": "fr",
+                "myst_enable_extensions": ["smartquotes"],
+            },
+            "Test\u2019s \u00ab\u00a0double\u00a0\u00bb and \u201csingle\u201d and \u00ab\u00a0emph\u00a0\u00bb",
+            id="fr-default",
+        ),
+        pytest.param(
+            '"Test"',
+            {
+                "language_code": "fr",
+                "smart_quotes": "alt",
+                "myst_enable_extensions": ["smartquotes"],
+            },
+            "\u00ab\u202fTest\u202f\u00bb",
+            id="fr-alt",
+        ),
+        pytest.param(
+            "---\nmyst:\n  enable_extensions: [smartquotes]\n---\n\"Hallo\" und 'Welt'",
+            {
+                "language_code": "de",
+            },
+            "\u201eHallo\u201c und \u201aWelt\u2018",
+            id="de-topmatter",
+        ),
+        pytest.param(
+            "\"Custom\" and 'quote'",
+            {
+                "language_code": "de",
+                "smartquotes_locales": [("de", ("[", "]", "{", "}"))],
+                "myst_enable_extensions": ["smartquotes"],
+            },
+            "[Custom] and {quote}",
+            id="custom-locales",
+        ),
+    ],
+)
+def test_docutils_smartquotes_localized(source, settings, expected):
+    """Docutils ``Parser`` localizes MyST ``smartquotes`` using document settings (#806)."""
+    doctree = publish_doctree(
+        source=source,
+        parser=Parser(),
+        settings_overrides={
+            "warning_stream": io.StringIO(),
+            **settings,
+        },
+    )
+    assert doctree.astext() == expected
diff --git a/tests/test_renderers/test_smartquotes.py b/tests/test_renderers/test_smartquotes.py
new file mode 100644
index 00000000..f38ce0d4
--- /dev/null
+++ b/tests/test_renderers/test_smartquotes.py
@@ -0,0 +1,145 @@
+"""Tests for localized quote rules with the MyST ``smartquotes`` extension (#806)."""
+
+from __future__ import annotations
+
+import pytest
+from docutils import nodes
+from docutils.utils.smartquotes import smartchars
+from sphinx_pytest.plugin import CreateDoctree
+
+
+@pytest.mark.parametrize(
+    ("language", "sphinx_smartquotes", "expected"),
+    [
+        pytest.param(
+            "fr",
+            True,
+            "Welcome to Test\u2019s documentation!\n\n\u00ab\u00a0Test\u00a0\u00bb and \u201csingle\u201d",
+            id="fr-with-sphinx-smartquotes",
+        ),
+        pytest.param(
+            "fr",
+            False,
+            "Welcome to Test\u2019s documentation!\n\n\u00ab\u00a0Test\u00a0\u00bb and \u201csingle\u201d",
+            id="fr-myst-only",
+        ),
+        pytest.param(
+            "de",
+            False,
+            "Welcome to Test\u2019s documentation!\n\n\u201eTest\u201c and \u201asingle\u2018",
+            id="de-myst-only",
+        ),
+        pytest.param(
+            "fr_CH",
+            False,
+            "Welcome to Test\u2019s documentation!\n\n\u00abTest\u00bb and \u2039single\u203a",
+            id="fr-ch-subtag",
+        ),
+        pytest.param(
+            "ja",
+            False,
+            "Welcome to Test\u2019s documentation!\n\n\u300cTest\u300d and \u300esingle\u300f",
+            id="ja-myst-only",
+        ),
+        pytest.param(
+            "ar",
+            False,
+            "Welcome to Test\u2019s documentation!\n\n\u201cTest\u201d and \u2018single\u2019",
+            id="unsupported-smartquotes-language-fallback",
+        ),
+    ],
+)
+def test_sphinx_smartquotes_language(
+    sphinx_doctree: CreateDoctree,
+    language: str,
+    sphinx_smartquotes: bool,
+    expected: str,
+) -> None:
+    """Sphinx ``language`` localizes MyST's ``smartquotes`` extension (#806)."""
+    sphinx_doctree.set_conf(
+        {
+            "extensions": ["myst_parser"],
+            "myst_enable_extensions": ["smartquotes"],
+            "language": language,
+            "smartquotes": sphinx_smartquotes,
+        }
+    )
+    result = sphinx_doctree(
+        "# Welcome to Test's documentation!\n\n\"Test\" and 'single'\n",
+        "index.md",
+    )
+    assert not result.warnings
+    assert result.doctrees["index"].astext() == expected
+
+
+def test_sphinx_smartquotes_topmatter_and_include(
+    sphinx_doctree: CreateDoctree,
+) -> None:
+    """Per-file front matter and ``{include}`` directives honor Sphinx ``language`` (#806)."""
+    sphinx_doctree.srcdir.joinpath("included.md").write_text(
+        "\"Included\" and 'nested'\n",
+        encoding="utf8",
+    )
+    sphinx_doctree.set_conf(
+        {
+            "extensions": ["myst_parser"],
+            "language": "fr",
+            "smartquotes": False,
+            "exclude_patterns": ["included.md"],
+        }
+    )
+    source = (
+        "---\n"
+        "myst:\n"
+        "  enable_extensions:\n"
+        "    - smartquotes\n"
+        "---\n"
+        "# Heading\n\n"
+        '"Main"\n\n'
+        "```{include} included.md\n"
+        "```\n"
+    )
+    result = sphinx_doctree(source, "index.md")
+    assert not result.warnings
+    paragraphs = [p.astext() for p in result.doctrees["index"].findall(nodes.paragraph)]
+    assert paragraphs == [
+        "\u00ab\u00a0Main\u00a0\u00bb",
+        "\u00ab\u00a0Included\u00a0\u00bb and \u201cnested\u201d",
+    ]
+
+
+def test_sphinx_smartquotes_env_locales_no_global_mutation(
+    sphinx_doctree: CreateDoctree,
+) -> None:
+    """Custom ``env.settings['smartquotes_locales']`` works without mutating Docutils globals."""
+    snapshot = dict(smartchars.quotes)
+    (sphinx_doctree.srcdir / "ext_locales.py").write_text(
+        "def setup(app):\n"
+        "    app.connect(\n"
+        "        'builder-inited',\n"
+        "        lambda app: app.env.settings.update({\n"
+        "            'smartquotes_locales': [('fr', ('[[', ']]', '{{', '}}'))],\n"
+        "        }),\n"
+        "    )\n",
+        encoding="utf8",
+    )
+    import sys
+
+    sys.path.insert(0, str(sphinx_doctree.srcdir))
+    try:
+        sphinx_doctree.set_conf(
+            {
+                "extensions": ["myst_parser", "ext_locales"],
+                "myst_enable_extensions": ["smartquotes"],
+                "language": "fr",
+                "smartquotes": False,
+            }
+        )
+        result = sphinx_doctree("# Title\n\n\"Double\" and 'single'\n", "index.md")
+    finally:
+        sys.path.remove(str(sphinx_doctree.srcdir))
+        sys.modules.pop("ext_locales", None)
+
+    assert not result.warnings
+    assert result.doctrees["index"].astext() == "Title\n\n[[Double]] and {{single}}"
+    assert smartchars.quotes == snapshot