diff --git a/.gitignore b/.gitignore
index 48df0e669..830b2c936 100644
--- a/.gitignore
+++ b/.gitignore
@@ -83,3 +83,4 @@ venv/
 
 # mypy
 .dmypy.json
+.mypy_cache
diff --git a/xonsh/ptk_shell/shell.py b/xonsh/ptk_shell/shell.py
index 3ec9f3316..90409613c 100644
--- a/xonsh/ptk_shell/shell.py
+++ b/xonsh/ptk_shell/shell.py
@@ -40,6 +40,7 @@ from prompt_toolkit.styles.pygments import (
 
 
 ANSI_OSC_PATTERN = re.compile("\x1b].*?\007")
+CAPITAL_PATTERN = re.compile(r"([a-z])([A-Z])")
 Token = _TokenType()
 
 events.transmogrify("on_ptk_create", "LoadEvent")
@@ -92,6 +93,18 @@ def remove_ansi_osc(prompt):
     return prompt, osc_tokens
 
 
+def _extract_ptk_style(pygments_style):
+    """Extract PTK specific rules that are not handled by ``style_from_pygments_cls``
+    """
+    rules = {}
+    for rule, value in pygments_style.styles.items():
+        if str(rule).startswith("Token.PTK"):
+            key = CAPITAL_PATTERN.sub(r"\1-\2", str(rule)[10:]).lower()
+            rules[key] = value
+
+    return rules
+
+
 class PromptToolkitShell(BaseShell):
     """The xonsh shell for prompt_toolkit v2 and later."""
 
@@ -201,7 +214,14 @@ class PromptToolkitShell(BaseShell):
         if env.get("COLOR_INPUT"):
             if HAS_PYGMENTS:
                 prompt_args["lexer"] = PygmentsLexer(pyghooks.XonshLexer)
-                style = style_from_pygments_cls(pyghooks.xonsh_style_proxy(self.styler))
+                style = merge_styles(
+                    [
+                        Style.from_dict(_extract_ptk_style(self.styler)),
+                        style_from_pygments_cls(
+                            pyghooks.xonsh_style_proxy(self.styler)
+                        ),
+                    ]
+                )
             else:
                 style = style_from_pygments_dict(DEFAULT_STYLE_DICT)
 
diff --git a/xonsh/pyghooks.py b/xonsh/pyghooks.py
index 630c10aa9..6adbe08d7 100644
--- a/xonsh/pyghooks.py
+++ b/xonsh/pyghooks.py
@@ -382,8 +382,8 @@ class XonshStyle(Style):
                 self.background_color = style_obj.background_color
             except (ImportError, pygments.util.ClassNotFound):
                 self._smap = XONSH_BASE_STYLE.copy()
-        compound = CompoundColorMap(ChainMap(self.trap, cmap, PTK_STYLE, self._smap))
-        self.styles = ChainMap(self.trap, cmap, PTK_STYLE, self._smap, compound)
+        compound = CompoundColorMap(ChainMap(self.trap, cmap, self._smap, PTK_STYLE))
+        self.styles = ChainMap(self.trap, cmap, self._smap, PTK_STYLE, compound)
         self._style_name = value
 
         for file_type, xonsh_color in builtins.__xonsh__.env.get(