@Kuba If you know the relative proportions Scaled works (e.g. Scaled[.9] and Scaled[.1]) but I'm not sure if there's a sense of "remaining" space in Mathematica's windowing system beyond something constructed via Dynamic
Agreed that it makes sense, but I think the Mathematica front-end is missing the necessary CSS-like flex constructions although you might be able to get a pure FE solution with some box-size trickery...