Among the emerging fungal diseases threatening food security, the Pseudocercospora fijiensis fungus causing black leaf streak disease of banana is one of the most marked examples of a recent worldwide pandemic on a major crop. We assessed how this pathogen spread throughout the latest invaded region, i.e. Central America and the Caribbean. We retraced its population history combining detailed monitoring information on disease outbreaks and population genetic analyses based on large-scale sampling of P. fijiensis isolates from 121 locations throughout the region. The results first suggested that sexual reproduction was not lost during the P. fijiensis expansion, even in the insular Caribbean context, and a high level of genotypic diversity was maintained in all the populations studied. The population genetic structure of P. fijiensis and historical data showed that two disease waves swept northward and southward in all banana-producing countries in the study area from an initial entry point in Honduras, probably mainly through gradual stepwise spore dispersal. Serial founder events accompanying the northern and southern waves led to the establishment of two different genetic groups. A different population structure was detected on the latest invaded islands (Martinique, Dominica and Guadeloupe), revealing multiple introductions and admixture events that may have been partly due to human activities. The results of this study highlight the need to step up surveillance to limit the spread of other known emerging diseases of banana spread mainly by humans, but also to curb gene flow between established pathogen populations which could increase their evolutionary potential.