The protistan parasite Perkinsus marinus causes Dermo disease in the eastern oyster, Crassostrea virginica. This parasite causes reduced growth and fecundity in its ecologically and economically important host, and as such has become a focal point for shellfish research. Though much is known regarding the seasonal dynamics and interactions between host and parasite, little research has focused on the basic biology of this parasite. In the research presented here, I used population genetic approaches to investigate the reproduction, dispersal, and origins of extant populations of P. marinus. First, I determined the extent of clonality in P. marinus populations. Repeated sampling of the same multilocus genotypes and extensive multilocus linkage disequilibrium indicated that clonal reproduction is prevalent. However, genotypic diversity was great and recombination occurred between genetic loci, supporting sexual reproduction as an important source of new genetic variation in P. marinus. An interesting consequence of sexual reproduction is that genotypic correlations may be maintained through inbreeding when sex occurs. Next, I investigated the genetic connectivity among locations. Clustering analyses revealed that local geographic samples are collections of independent clonal lineages rather than freely interbreeding populations. Some lineages were widespread while others were found at high frequencies only in specific locations indicating that P. marinus has a high capacity for dispersal, but local conditions may determine the success of certain lineages. Finally, I examined an interesting pattern of di-allelism observed in P. marinus DNA sequences. Two allelic classes were discovered at six out of seven nuclear loci where large divergences indicated the alleles had been independent for possibly millions of years. Balancing selection may be responsible for the retention of ancient diversity in this parasite, but it seems more likely that a recent hybridization event has occurred between two formerly allopatric lineages. These results underscore risks in the anthropogenic movement of protistan parasites as there may be no reproductive barriers between ancient lineages. Resulting hybrids could result in increased parasite virulence with increased disease in host populations.