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White pine blister rust, Cronartium ribicola (Basidiomycota, Pucciniales), is a macrocyclic (5 different spore types) heteroecious (requires two hosts) rust that alternates on Ribes spp. It is an exotic pathogen in North America and cause high levels of mortality of pine in the subsection Strobus (white pines). To better understand the epidemiology of the pathogen, the population structure of white pine blister rust in North America was investigated. Thirty one single nucleotide polymorphism (SNP) markers have been developed to genotype 1341 individuals from 76 populations from across North America including samples from diverse landscapes. In western Canada, sampling was structured to contrast different landscapes and pine hosts. Distance-based and Bayesian likelihood methods indicated the presence of two major genetic clusters: ‘eastern’ and ‘western’ in North America, separated by the Great Plains that act as a barrier to gene flow. The eastern cluster had greater genetic diversity than the western cluster, which confirms that multiple introductions occurred in eastern North America in contrast to a single introduction in the west. Two populations, New Mexico and Minnesota were each found to form a separate cluster in some assignment analyses and the distance-based analyses clearly placed them outside of the main clusters. Both of these populations displayed the hallmarks of a founder effect, i.e. low genetic diversity and/or inbreeding. The pathogen was discovered in New Mexico in the 1970’s, almost a century later than the populations in the two major clusters. Although white pine blister rust has been present for longer in Minnesota, the population parameters strongly suggest a founder effect and a barrier to gene flow between Minnesota and the populations within the eastern cluster. However, no landscape, host, or other patterns could be correlated with these clusters. A rare SNP was detected in Smithers, a population with high levels of inbreeding located at the northern most extent of the rust. Understanding the population structure will provide great knowledge of the rust for breeding programs and deployment of rust resistant pines.