In this paper, we provide upper and lower bounds on the crossing numbers of dense graphs on surfaces, which match up to constant factors. First, we prove that if $G$ is a dense enough graph with $m$ edges and $Σ$ is a surface of genus $g$, then any drawing of $G$ on $Σ$ incurs at least $Ω\left(\frac{m^2}{g} \log ^2 g\right)$ crossings. The poly-logarithmic factor in this lower bound is new even in the case of complete graphs and disproves a conjecture of Shahrokhi, Székely and Vrt'o from 1996. Then we prove a geometric converse to this lower bound: we provide an explicit family of hyperbolic surfaces such that for any graph $G$, sampling the vertices uniformly at random on this surface and connecting them with shortest paths yields $O\left(\frac{m^2}{g} \log ^2 g\right)$ crossings in expectation.