Spat collecting of the black lip oyster (Pinctada margaritifera) is the foundation of cultured black pearl production, the second source of income for French Polynesia. To understand spat collecting temporal and spatial variations, larval supply and its origin need to be characterized. To achieve this, it is necessary to account for the stock of oysters, its distribution and population characteristics (size distribution, sex-ratio). While the farmed stock in concessions can be easily characterized, the wild stock is elusive. Here, we investigate the distribution and population structure of the wild stock of Ahe and Takaroa atolls using fine-scale bathymetry and in situ census data. Stocks were surprisingly low (∼666,000 and ∼1,030,000 oysters for Ahe and Takaroa respectively) considering these two atolls have both been very successful spat collecting atolls in the past. Furthermore, in Ahe atoll, wild populations are aging with a dominant but small female population. Comparison with the cultured stock population (∼14 millions oysters) and its dominant young male population suggests that to maximize larval supply and spat collecting on the long term, it would be useful to increase the number of females in selected sanctuaries. We discuss the implication of our findings for the long-term management of stocks and for spat collection in pearl farming atolls, and for on-going numerical modelling studies on larval dispersal.