Frosty pod rot disease of cacao (FPR), caused by the fungus Moniliophthora roreri, has severely impacted the production of cocoa in Latin America since its discovery. Prior to the 1950s, FPR was known only from Colombia and Ecuador. However, beginning in the 1970s, its geographical range has dramatically expanded throughout most of the cacao-producing regions of the Americas. The origin of the pathogen remains unknown. In this study, we evaluated the genetic diversity of M. roreri from areas spanning, as much as possible, its current geographical range using simple-sequence repeat markers and a publicly available single-nucleotide polymorphism data set. Two hotspots of genetic diversity were found: coastal Ecuador and the inter-Andean Magdalena Valley of Colombia, neither of which correspond to the Amazonian origin of the host. However, both areas were early centres of intense cultivation of cacao. Our results indicate that M. roreri was introduced into both areas from its centre of origin, where intensive cacao cultivation probably led to the increase of inoculum and further dissemination of the disease. Current invasions can be traced to two genotypes responsible for all known instances of the pathogen in Central America, the Caribbean, Peru and Bolivia. We also report for the first time M. roreri in Maynas (Peruvian Amazon), which is probably the result of a recent introduction from Colombia.