Whole genome resequencing of 25 isolates of the ascomycete pine pathogen Dothistroma septosporum revealed the presence of three genetically distinct races in Scotland, confirming previous results based on microsatellite markers. The genetically uniform indigenous race from Scotland (NPR), is closely related to an introduced and genetically diverse southern race (SR) from England and France. Race LPR, confined to lodgepole pine, is genetically divergent from these, but has close affinity with Canadian (CAN) isolates. Genome comparisons between individuals within CAN and SR races revealed short and scattered regions of near sequence identity, indicating significant sexual reproduction. Sequence identity patterns within LPR suggest that it derives from introduction of a single sexual fruit body from North America. Finally a first generation interracial hybrid between indigenous NPR and introduced SR was identified, signalling an increase in the evolutionary potential of D. septosporum in Scotland, and an enhanced risk to native Scots pine (Pinus sylvestris).