Butterfly migration across great distances is testimony to their impressive aeronautical skills. Wing size and shape are two key determinants of flight performance, and in butterflies, the specific configuration of forewings to hindwings including the overlapping area between them can have profound effects on overall size and shape. Here we use quantitative morphometrics to analyze the wing size, shape, and flight performance of 190 exemplar species representing a tribal-level phylogeny of Papilionoidea. We identify three morphological ‘flight systems’ that are characterized by these fore- and hindwing configurations (small [beating], medium, and large [gliding]), and our data suggest that the emergence of these systems coincided with periods of paleoclimatic upheaval. A higher proportion of migratory species have wings characteristic of gliders, and their degree of host specialization appears to be more flexible than that of counterparts with beating wings.