The release of captive-bred plants and animals has increased worldwide to augment declining species. However, insufficient attention has been given to understanding how neutral and adaptive genetic variation are partitioned within and among proximal natural populations, and the patterns and drivers of gene flow over small spatial scales, which can be important for restoration success. A seascape genomics approach was used to investigate population structure, local adaptation, and the extent to which environmental gradients influence genetic variation among natural and restored populations of Chesapeake Bay eastern oysters Crassostrea virginica. We also investigated the impact of hatchery practices on neutral genetic diversity of restored reefs and quantified the broader genetic impacts of large-scale hatchery-based bivalve restoration. Restored reefs showed similar levels of diversity as natural reefs, and striking relationships were found between planting frequency and broodstock numbers and genetic diversity metrics (effective population size and relatedness), suggesting that hatchery practices can have a major impact on diversity. Despite long-term restoration activities, haphazard historical translocations, and high dispersal potential of larvae that could homogenize allele frequencies among populations, moderate neutral population genetic structure was uncovered. Moreover, environmental factors, namely salinity, pH, and temperature, play a major role in the distribution of neutral and adaptive genetic variation. For marine invertebrates in heterogeneous seascapes, collecting broodstock from large populations experiencing similar environments to candidate sites may provide the most appropriate sources for restoration and ensure population resilience in the face of rapid environmental change. This is one of a few studies to demonstrate empirically that hatchery practices have a major impact on the retention of genetic diversity. Overall, these results contribute to the growing body of evidence for fine-scale genetic structure and local adaptation in broadcast-spawning marine species and provide novel information for the management of an important fisheries resource.