Use a GtkSeparator to separate the stack sidebar from the various demo widgets, use custom styling to make the sidebar not draw its own separator, and move the start of the header bar and the header bar separator out of their box and directly into the leaflet.
This allows to have the separators well aligned with no workaround other than a simple custom style, to have no separator appearing when the window is folded, and to not trigger the GTK+ bug making titlebar separators appear black.