Geomorphological features of atolls in the Tuamotu archipelago (French Polynesia) created during glaciation periods of the Pleistocene enable unique studies of evolution. Atolls not far from one another may be classic open atolls with water exchange between the ocean and the lagoon, or they may have an enclosed lagoon, without a direct ocean connection since at least the last glaciation (20,000 yr ago). Niau’s atoll has an enclosed lagoon that hosts a milkfish (Chanos chanos) population whose origin is enigmatic. The milkfish’s cooccurrence with a tilapia species suggests a human introduction. However, there is no such record, and the people of Niau consider the milkfish population origin to be natural. The fish is used as staple food, and it also plays a major role in several of their cultural traditions. We compared genetic diversity and population history of the Niau milkfish to those of the milkfish of a nearby open atoll, Kauehi, using a mitochondrial marker. Niau’s milkfish population exhibits a lower genetic diversity compared to that of the Kauehi population, suggesting that the population experienced a genetic bottleneck. However, the two populations are not differentiated, consistent with the hypothesis that Niau’s milkfish population origin is human derived from the surrounding ocean population. Its smaller effective size suggests that this population has been self-sustaining for many generations. Ancient Polynesians were known for their transport of many species throughout the Pacific; this study is the first case suggesting transplantation of a marine fish. In addition, our results suggest that Niau’s milkfish population is large enough to limit inbreeding depression and seems to have been effectively managed over multiple generations by the local Polynesian communities.