Sorry for the noise, I've solved it, turns out makeup pages still have headers which you need to set to zero if you want uniform margins:
% Title page layout
% \definemakeup defines a layout with the same name, which we alter.
\definemakeup[titlepage]
\setuplayout [titlepage][width=middle, backspace=20mm,
height=middle, topspace=20mm,
header=0mm]
did the trick for me.
Incidentally, what threw me off was the phrasing in the manual:
4.19
Makeup
A document may have a titlepage, a colofon and some pages that are not directly related to the
main part of the document. Mostly these pages are not numbered and can do without headers
and footers. Because their layout needs extra attention we prefer the word makeup for defining
their specific layout.
Since my makeup pages indeed don't have page numbers, I presumed they wouldn't have headers either. I may have read too much into that, but perhaps that passage can be improved?