Phylogenomic analyses of datasets comprising 665 anchored loci and 234 species representing all recognized tribes and regional faunas of the leafhopper subfamily Typhlocybinae yielded well-resolved phylogenies for this group, largely robust to differences in analytical approach. The results support the 5 currently recognized tribes as monophyletic: Alebrini, Empoascini, Typhlocybini, Dikraneurini, and Erythroneurini, but the previously recognized tribes Zyginellini and Eupterygini are polyphyletic. A new tribe Beameranini is described based on the morphologically aberrant Neotropical genus Beamerana Young. Morphological characters traditionally used to recognize tribes are mostly stable but nearly all exhibit some homoplasy, with similar reductions and consolidations of some hind wing veins having occurred in independent lineages. Divergence time estimates indicate that the currently recognized tribes all arose during the mid- to late Cretaceous with some early splits between New and Old World lineages occur during the late Cretaceous, but most modern genera arising during the Paleogene and multiple transcontinental dispersal events also occur in the Paleogene.