Translocation has been widely studied as a tool for conservation management to restore or enhance degraded populations. On the contrary, few studies have been conducted on translocation for commercial purposes. In this study, we evaluate the genetic consequences of translocation of wild individuals of Pinctada margaritifera on farmed and adjacent wild populations. We tested the hypotheses that translocations would induce high genetic heterogeneity in farmed populations and this heterogeneity would then leak into the adjacent wild populations. In fact, farmed samples exhibit high levels of heterogeneity and low pairwise relatedness compared to wild populations, highlighting the pooling of genetically divergent populations into farms. We also demonstrate that this heterogeneity is transmitted to adjacent wild populations as a result of interbreeding. Adjacent wild populations tend to have higher genetic diversity values and greater pairwise relatedness coefficient with farmed populations than wild populations. Overall, pearl culture in French Polynesia promotes the mixing of unrelated individuals in farmed locations and reduces genetic divergence among geographically distant populations as well as among farmed and wild populations of a same lagoon. We also studied for the first time a farmed population originating from spat collected in a lagoon where release of hatchery-produced larvae occurred 10 years ago and we were able to identify four distinct genetic groups. These groups contribute highly to reproduction and caused considerable genetic drift in the lagoon, suggesting that hatchery-produced larvae are neither sustainable method for pearl culture nor for conserving the diversity of P. margaritifera in French Polynesia.