Acanthoscelides obtectus Say is a bruchid species of Neotropical origin, and is specialized on beans of the Phaseolus vulgaris L. group. Since the domestication and diffusion of beans, A. obtectus has become cosmopolitan through human-mediated migrations and is now a major pest in bean granaries. Using phylogeographic methods applied to mitochondrial DNA (mtDNA) and nuclear microsatellite molecular markers, we show that the origin of this species is probably further south than Mesoamerica, as commonly thought. Our results also indicate that A. obtectus and its Mesoamerican sister species Acanthoscelides obvelatus, two morphologically close species differing principally in voltinism, speciated in allopatry: A. obtectus (multivoltine) arising in Andean America and A. obvelatus (univoltine) in Mesoamerica. In contrast to Mesoamerica where beans fruit once yearly, wild beans in Andean America fruit year-round, especially in regions showing little or no seasonality. In such habitats where resources are continuously present, multivoltinism is adaptive. According to existing hypotheses, multivoltinism in A. obtectus is a new adaptation that evolved after bean domestication. Our data suggest the alternative hypothesis that multivoltinism is an older trait, adapted to exploit the year-round fruiting of wild beans in relatively aseasonal habitats, and allowed A. obtectus to become a pest in bean granaries. This trait also permitted this species to disperse through human-mediated migrations associated with diffusion of domesticated beans. We also show that diversity of Old World A. obtectus populations can be quite well explained by a single colonization event about 500 BP. Human-mediated migrations appear not to be rare, as our results indicate a second more recent migration event from Andean America to Mexico.