True crocodiles (Crocodylus) are the most broadly distributed, ecologically diverse, and species-rich crocodylian genus, comprising about half of extant crocodylian diversity and exhibiting a circumtropical distribution. Crocodylus traditionally has been viewed as an ancient group of morphologically conserved species that originated in Africa prior to continental breakup. In this study, these long-held notions about the temporal and geographic origin of Crocodylus are tested using DNA sequence data of 10 loci from 76 individuals representing all 23 crocodylian species. I infer a time-calibrated species tree of all Crocodylia and estimate the spatial pattern of diversification within Crocodylus. For the first time, a fully resolved phylogenetic estimate of all Crocodylia is well-supported. The results overturn traditional views of the evolution of Crocodylus by demonstrating that the true crocodiles are not “living-fossils” that originated in Africa. Rather, Crocodylus originated from an ancestor in the tropics of the Late Miocene Indo-Pacific, and rapidly radiated and dispersed around the globe during a period marked by mass extinctions of fellow crocodylians. The findings also reveal more diversity within the genus than is recognized by current taxonomy.