The eastern oyster, Crassostrea virginica, plays an important role in the ecology of Chesapeake Bay. Its large population size, long larval dispersal stage and potential for high variance in reproductive success is representative of many marine invertebrates. Nevertheless, many important aspects of the oyster’s biology remain unclear. I investigated how migration, natural selection, and effective population size have shaped the evolution of Chesapeake oysters. First, I examined aspects of genetic connectivity among oysters from rivers throughout the Bay. A correlation between geographic and genetic distance indicated that oyster larval dispersal tends to be local and that migration between Bay tributaries is rare over an ecological time scale. This result contributes to a growing body of literature indicating that larval dispersal is not passive. Next, I showed that a pattern of non-neutral mitochondrial evolution previously observed in different oyster populations also existed in Chesapeake Bay C. virginica. Tests of selection indicated that the pattern, in which there is an excess of high frequency and low frequency haplotypes and a deficit of intermediate frequency haplotypes, was the result of positive selection on the genome. Demographic explanations appear unlikely to account for the mitochondrial haplotype pattern because nuclear loci exhibited neutral patterns of sequence evolution. Estimates of effective population size were several orders of magnitude smaller than census size, indicating that there was variance in reproductive success (sweepstakes reproduction). Nevertheless sweepstakes reproduction was not so severe that individual cohorts of juvenile oysters exhibited reduced levels of variation compared to the adult population. Finally I evaluated the risks associated with a supplementation program in which hatchery-raised oysters bred for disease tolerance were released into wild oyster populations. The results indicated that following supplementation, the wild effective population size remained large despite the danger of severe genetic bottlenecks. Increased hatchery effective population is suggested to prevent future harm to the wild population.