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Preserving and maximizing genetic diversity in conservation programs, including for restocking, are of high importance. The threatened European flat oyster (Ostrea edulis) is currently the subject of several applied conservation and restocking programs, but concerns have been raised over potential negative side effects of these programs, for example due to our limited knowledge about the genetic effects in natural populations of releasing offspring of hatchery origin. Here, we developed an effective, easily applicable and highly reliable method to assess the genetic diversity and parental contributions in flat oyster hatchery production based on analyses of 17 microsatellite loci. We analysed four broodstocks and their hatchery-reared spat (total n = 354) and compared diversity to that in wild samples of adults and spat from the broodstock source in the Limfjorden (total n = 138). Based on four hatchery tank experiments with fully resolved parentage assignments, we found that five swarming events (larval releases) were characterized by a single maternal and multiple paternal contributions, and that the number of contributing parents varied greatly both among individual tanks, and between swarming events within tank. On average, the effective number of breeders was only one third of the actual broodstock size. Although the broodstock exhibited high genetic variation, the high reproductive skew resulted in produced offspring representing only a relatively small subset of this variation. The work demonstrates potential impact of hatchery reared offspring on decreasing genetic diversity in wild populations, but also that genetic monitoring can be integrated in conservation programs to minimize negative effects on restoration and supplementary restocking programs that utilize hatchery reared spats to support natural populations.