As the agent of Dermo disease, Perkinsus marinus causes significant mortality and reduced fecundity its eastern oyster host, Crassostrea virginica. Passive dispersal of P. marinus between hosts subjects parasite movements to control by water currents in estuarine systems, potentially limiting connectivity among parasite populations in different estuaries. Given recent evidence for sexual reproduction in P. marinus, estimates of gene flow among locations may provide insights into this parasite's epidemiology. In this study, 1,082 wild oysters were collected from 2002 to 2008 at 15 geographical locations encompassing 4,800 km of the Gulf of Mexico and Atlantic coasts of the United States. Of these, 742 oysters (68.9% prevalence) were determined to be infected by P. marinus. Among infected oysters, 374 were determined to be infected by a single parasite genotype based on amplification of seven microsatellite loci, and therefore were amenable to analysis. Allele frequencies differed significantly among most locales, but there was no indication of isolation by distance. Four distinct clusters of multilocus genotypes were identified by analyzing genetic distances among individuals and by using Bayesian assignment tests. One lineage occurred in many locations, whereas the others were limited to a particular region or disjunct locations. Two lineages were associated with recent range expansion. Altogether, local assemblages of P. marinus are characterized by mixtures of distinct sympatric populations that undergo only infrequent recombination. By mixing divergent strains, long-distance dispersal and/or anthropogenic introduction may play an important role in the evolution of P. marinus and spread of Dermo disease, whereas locally, high-frequency strains may represent focal epizootics.