The powdery mildew pathogen Podosphaera macularis can devastate commercial hops. The fungus was unknown in the Pacific Northwestern US, the primary hop production region in this country, until the mid-1990s. The disease has occasionally been reported in other regions of the eastern US as hop production has reestablished. We sequenced transcriptomes of 104 isolates collected throughout the US and Europe to better understand genetic diversity of the fungus and the possible origin of the population in the western US. Discriminant analysis of principle components grouped isolates into 3 to 5 geographic populations, dependent on stringency of the grouping criteria. Western US isolates were clonal, irrespective of pathogenic race, and consistently grouped with isolates from Europe. Eastern US isolates from wild hops were genetically unique, however isolates from cultivated hops in the eastern US were most often genetically similar to western US isolates. Mating types of isolates originating from cultivated western and eastern US hop were invariably MAT1-1. In contrast, a 1:1 ratio of MAT1-1 and MAT1-2 was observed with isolates from wild plants or Europe. The foregoing genetic and phenotypic patterns suggests a European origin of P. macularis populations in the western US, followed by spread of the pathogen from the western US to re-emergent production regions in the eastern US, perhaps via distribution on planting material.