The rapid growth of the aquaculture industry to meet global seafood demand offers both risks and opportunities for resource management and conservation. In particular, hatcheries hold promise for stock enhancement and restoration, yet cultivation practices may lead to enhanced variation between populations at the expense of variation within populations, with uncertain implications for performance and resilience. To date, few studies have assessed how production techniques impact genetic diversity and population structure, as well as resultant trait variation in and performance of cultivated offspring. We collaborated with a commercial hatchery to produce multiple cohorts of the eastern oyster (Crassostrea virginica) from field‐collected broodstock using standard practices. We recorded key characteristics of the broodstock (male : female ratio, effective population size), quantified the genetic diversity of the resulting cohorts, and tested their trait variation and performance across multiple field sites and experimental conditions. Oyster cohorts produced under the same conditions in a single hatchery varied almost twofold in genetic diversity. In addition, cohort genetic diversity was a significant positive predictor of oyster performance traits, including initial size and survival in the field. Oyster cohorts produced in the hatchery had lower within‐cohort genetic variation and higher among‐cohort genetic structure than adults surveyed from the same source sites. These findings are consistent with “sweepstakes reproduction” in oysters, even when manually spawned. A readily measured characteristic of broodstock, the ratio of males to females, was positively correlated with within‐cohort genetic diversity of the resulting offspring. Thus, this metric may offer a tractable way both to meet short‐term production goals for seafood demand and to ensure the capacity of hatchery‐produced stock to achieve conservation objectives, such as the recovery of self‐sustaining wild populations.