Population genetic structure in the presence of substantial dispersal provides a unique perspective on the evolution of reproductive isolation. We sampled Telmatherina antoniae, an endemic fish species, at 10 sites in Lake Matano, Indonesia. Significant genetic structure (FST = 0.03) was found, despite a migration rate of 10.2% and a mean dispersal distance of 13.6 km, estimated by genotype assignment. Neither dispersal distance nor direction differed from random expectations, indicative of no dispersal barrier in Lake Matano. However, Bayesian genotype cluster assignment identified a population structure consisting of four to six clusters that did not coincide with sample site distribution, but explained two to three times more genetic variance than sample site. The mechanism for continued isolation of those genetic clusters is unknown, but assortative mating and temporal isolation are obvious candidates. Our results resolve the apparent paradox of population genetic structure coupled with frequent dispersal, and highlight the importance of considering cryptic genetic structure.