diff --git a/Lib/idlelib/codecontext.py b/Lib/idlelib/codecontext.py
index b061f3b2fe8..78edf12263a 100644
--- a/Lib/idlelib/codecontext.py
+++ b/Lib/idlelib/codecontext.py
@@ -20,7 +20,7 @@ from idlelib.config import idleConf
 BLOCKOPENERS = {"class", "def", "elif", "else", "except", "finally", "for",
                 "if", "try", "while", "with", "async"}
 UPDATEINTERVAL = 100 # millisec
-FONTUPDATEINTERVAL = 1000 # millisec
+CONFIGUPDATEINTERVAL = 1000 # millisec
 
 
 def get_spaces_firstword(codeline, c=re.compile(r"^(\s*)(\w*)")):
@@ -45,9 +45,6 @@ def get_line_info(codeline):
 class CodeContext:
     "Display block context above the edit window."
 
-    bgcolor = "LightGray"
-    fgcolor = "Black"
-
     def __init__(self, editwin):
         """Initialize settings for context block.
 
@@ -69,22 +66,20 @@ class CodeContext:
         self.editwin = editwin
         self.text = editwin.text
         self.textfont = self.text["font"]
+        self.contextcolors = CodeContext.colors
         self.label = None
         self.topvisible = 1
         self.info = [(0, -1, "", False)]
         # Start two update cycles, one for context lines, one for font changes.
         self.t1 = self.text.after(UPDATEINTERVAL, self.timer_event)
-        self.t2 = self.text.after(FONTUPDATEINTERVAL, self.font_timer_event)
+        self.t2 = self.text.after(CONFIGUPDATEINTERVAL, self.config_timer_event)
 
     @classmethod
     def reload(cls):
         "Load class variables from config."
         cls.context_depth = idleConf.GetOption("extensions", "CodeContext",
                                        "maxlines", type="int", default=15)
-##        cls.bgcolor = idleConf.GetOption("extensions", "CodeContext",
-##                                     "bgcolor", type="str", default="LightGray")
-##        cls.fgcolor = idleConf.GetOption("extensions", "CodeContext",
-##                                     "fgcolor", type="str", default="Black")
+        cls.colors = idleConf.GetHighlight(idleConf.CurrentTheme(), 'context')
 
     def __del__(self):
         "Cancel scheduled events."
@@ -118,7 +113,8 @@ class CodeContext:
             self.label = tkinter.Label(
                     self.editwin.top, text="",
                     anchor=W, justify=LEFT, font=self.textfont,
-                    bg=self.bgcolor, fg=self.fgcolor,
+                    bg=self.contextcolors['background'],
+                    fg=self.contextcolors['foreground'],
                     width=1,  # Don't request more than we get.
                     padx=padx, border=border, relief=SUNKEN)
             # Pack the label widget before and above the text_frame widget,
@@ -202,13 +198,17 @@ class CodeContext:
             self.update_code_context()
         self.t1 = self.text.after(UPDATEINTERVAL, self.timer_event)
 
-    def font_timer_event(self):
-        "Event on editor text widget triggered every FONTUPDATEINTERVAL ms."
+    def config_timer_event(self):
+        "Event on editor text widget triggered every CONFIGUPDATEINTERVAL ms."
         newtextfont = self.text["font"]
-        if self.label and newtextfont != self.textfont:
+        if (self.label and (newtextfont != self.textfont or
+                            CodeContext.colors != self.contextcolors)):
             self.textfont = newtextfont
+            self.contextcolors = CodeContext.colors
             self.label["font"] = self.textfont
-        self.t2 = self.text.after(FONTUPDATEINTERVAL, self.font_timer_event)
+            self.label['background'] = self.contextcolors['background']
+            self.label['foreground'] = self.contextcolors['foreground']
+        self.t2 = self.text.after(CONFIGUPDATEINTERVAL, self.config_timer_event)
 
 
 CodeContext.reload()
diff --git a/Lib/idlelib/config-highlight.def b/Lib/idlelib/config-highlight.def
index 4146e28c4ed..aaa2b57a7f6 100644
--- a/Lib/idlelib/config-highlight.def
+++ b/Lib/idlelib/config-highlight.def
@@ -31,6 +31,8 @@ stderr-foreground= red
 stderr-background= #ffffff
 console-foreground= #770000
 console-background= #ffffff
+context-foreground= #000000
+context-background= lightgray
 
 [IDLE New]
 normal-foreground= #000000
@@ -62,6 +64,8 @@ stderr-foreground= red
 stderr-background= #ffffff
 console-foreground= #770000
 console-background= #ffffff
+context-foreground= #000000
+context-background= lightgray
 
 [IDLE Dark]
 comment-foreground = #dd0000
@@ -91,3 +95,5 @@ stdout-background = #002240
 hit-foreground = #002240
 comment-background = #002240
 break-foreground = #FFFFFF
+context-foreground= #ffffff
+context-background= #454545
diff --git a/Lib/idlelib/config.py b/Lib/idlelib/config.py
index c3e57bc692d..94b20832091 100644
--- a/Lib/idlelib/config.py
+++ b/Lib/idlelib/config.py
@@ -360,6 +360,8 @@ class IdleConf:
                 'stderr-background':'#ffffff',
                 'console-foreground':'#000000',
                 'console-background':'#ffffff',
+                'context-foreground':'#000000',
+                'context-background':'#ffffff',
                 }
         for element in theme:
             if not cfgParser.has_option(themeName, element):
diff --git a/Lib/idlelib/configdialog.py b/Lib/idlelib/configdialog.py
index 28ad4586394..7df69d5c4d6 100644
--- a/Lib/idlelib/configdialog.py
+++ b/Lib/idlelib/configdialog.py
@@ -799,19 +799,20 @@ class HighPage(Frame):
         """
         self.theme_elements = {
             'Normal Text': ('normal', '00'),
-            'Python Keywords': ('keyword', '01'),
-            'Python Definitions': ('definition', '02'),
-            'Python Builtins': ('builtin', '03'),
-            'Python Comments': ('comment', '04'),
-            'Python Strings': ('string', '05'),
-            'Selected Text': ('hilite', '06'),
-            'Found Text': ('hit', '07'),
-            'Cursor': ('cursor', '08'),
-            'Editor Breakpoint': ('break', '09'),
-            'Shell Normal Text': ('console', '10'),
-            'Shell Error Text': ('error', '11'),
-            'Shell Stdout Text': ('stdout', '12'),
-            'Shell Stderr Text': ('stderr', '13'),
+            'Code Context': ('context', '01'),
+            'Python Keywords': ('keyword', '02'),
+            'Python Definitions': ('definition', '03'),
+            'Python Builtins': ('builtin', '04'),
+            'Python Comments': ('comment', '05'),
+            'Python Strings': ('string', '06'),
+            'Selected Text': ('hilite', '07'),
+            'Found Text': ('hit', '08'),
+            'Cursor': ('cursor', '09'),
+            'Editor Breakpoint': ('break', '10'),
+            'Shell Normal Text': ('console', '11'),
+            'Shell Error Text': ('error', '12'),
+            'Shell Stdout Text': ('stdout', '13'),
+            'Shell Stderr Text': ('stderr', '14'),
             }
         self.builtin_name = tracers.add(
                 StringVar(self), self.var_changed_builtin_name)
@@ -842,6 +843,7 @@ class HighPage(Frame):
             ('\n', 'normal'),
             ('#you can click here', 'comment'), ('\n', 'normal'),
             ('#to choose items', 'comment'), ('\n', 'normal'),
+            ('code context section', 'context'), ('\n\n', 'normal'),
             ('def', 'keyword'), (' ', 'normal'),
             ('func', 'definition'), ('(param):\n  ', 'normal'),
             ('"""string"""', 'string'), ('\n  var0 = ', 'normal'),
diff --git a/Lib/idlelib/idle_test/test_codecontext.py b/Lib/idlelib/idle_test/test_codecontext.py
index 4c775eee6b5..d446090b082 100644
--- a/Lib/idlelib/idle_test/test_codecontext.py
+++ b/Lib/idlelib/idle_test/test_codecontext.py
@@ -110,6 +110,8 @@ class CodeContextTest(unittest.TestCase):
 
     def test_reload(self):
         codecontext.CodeContext.reload()
+        self.assertEqual(self.cc.colors, {'background': 'lightgray',
+                                          'foreground': '#000000'})
         self.assertEqual(self.cc.context_depth, 15)
 
     def test_toggle_code_context_event(self):
@@ -125,8 +127,8 @@ class CodeContextTest(unittest.TestCase):
         eq(toggle(), 'break')
         self.assertIsNotNone(cc.label)
         eq(cc.label['font'], cc.textfont)
-        eq(cc.label['fg'], cc.fgcolor)
-        eq(cc.label['bg'], cc.bgcolor)
+        eq(cc.label['fg'], cc.colors['foreground'])
+        eq(cc.label['bg'], cc.colors['background'])
         eq(cc.label['text'], '')
 
         # Toggle off.
@@ -275,11 +277,13 @@ class CodeContextTest(unittest.TestCase):
         self.cc.timer_event()
         mock_update.assert_called()
 
-    def test_font_timer_event(self):
+    def test_config_timer_event(self):
         eq = self.assertEqual
         cc = self.cc
         save_font = cc.text['font']
+        save_colors = codecontext.CodeContext.colors
         test_font = 'FakeFont'
+        test_colors = {'background': '#222222', 'foreground': '#ffff00'}
 
         # Ensure code context is not active.
         if cc.label:
@@ -287,24 +291,42 @@ class CodeContextTest(unittest.TestCase):
 
         # Nothing updates on inactive code context.
         cc.text['font'] = test_font
-        cc.font_timer_event()
+        codecontext.CodeContext.colors = test_colors
+        cc.config_timer_event()
         eq(cc.textfont, save_font)
+        eq(cc.contextcolors, save_colors)
 
-        # Activate code context, but no change to font.
+        # Activate code context, but no change to font or color.
         cc.toggle_code_context_event()
         cc.text['font'] = save_font
-        cc.font_timer_event()
+        codecontext.CodeContext.colors = save_colors
+        cc.config_timer_event()
         eq(cc.textfont, save_font)
+        eq(cc.contextcolors, save_colors)
         eq(cc.label['font'], save_font)
+        eq(cc.label['background'], save_colors['background'])
+        eq(cc.label['foreground'], save_colors['foreground'])
 
         # Active code context, change font.
         cc.text['font'] = test_font
-        cc.font_timer_event()
+        cc.config_timer_event()
         eq(cc.textfont, test_font)
+        eq(cc.contextcolors, save_colors)
         eq(cc.label['font'], test_font)
+        eq(cc.label['background'], save_colors['background'])
+        eq(cc.label['foreground'], save_colors['foreground'])
 
+        # Active code context, change color.
         cc.text['font'] = save_font
-        cc.font_timer_event()
+        codecontext.CodeContext.colors = test_colors
+        cc.config_timer_event()
+        eq(cc.textfont, save_font)
+        eq(cc.contextcolors, test_colors)
+        eq(cc.label['font'], save_font)
+        eq(cc.label['background'], test_colors['background'])
+        eq(cc.label['foreground'], test_colors['foreground'])
+        codecontext.CodeContext.colors = save_colors
+        cc.config_timer_event()
 
 
 class HelperFunctionText(unittest.TestCase):
diff --git a/Misc/NEWS.d/next/IDLE/2018-05-29-07-14-37.bpo-33679.MgX_Ui.rst b/Misc/NEWS.d/next/IDLE/2018-05-29-07-14-37.bpo-33679.MgX_Ui.rst
new file mode 100644
index 00000000000..43d78b023f6
--- /dev/null
+++ b/Misc/NEWS.d/next/IDLE/2018-05-29-07-14-37.bpo-33679.MgX_Ui.rst
@@ -0,0 +1,12 @@
+IDLE: Re-enable color configuration for Code Context.
+The difference from before is that the settings are now on the
+Highlights tab instead of the Extensions tab and only change one theme
+at a time instead of all themes.  The default for light themes is black
+on light gray, as before.  The default for the IDLE Dark theme is white
+on dark gray, which better fits the dark theme.
+
+When one starts IDLE from a console and loads a custom theme without
+definitions for 'context', one will see a warning message on the console.
+To stop the warning, go to Options => Configure IDLE => Highlights,
+select the custom theme if not selected already, select 'Code Context',
+and select foreground and background colors.