Phenotypic plasticity in life-history traits in response to heterogeneous environments has been observed in a number of fishes. Conversely, genetic structure has recently been detected in even the most wide ranging pelagic teleost fish and shark species with massive dispersal potential, putting into question previous expectations of panmixia. Shallow oceanic seamounts are known aggregation sites for pelagic species, but their role in genetic structuring of widely distributed species remains poorly understood. The yellowtail kingfish (Seriola lalandi), a commercially valuable, circumglobal, epipelagic fish species occurs in two genetically distinct Southern Hemisphere populations (South Pacific and southern Africa) with low levels of gene-flow between the regions. Two shallow oceanic seamounts exist in the ocean basins around southern Africa; Vema and Walters Shoal in the Atlantic and Indian oceans, respectively. We analysed rare samples from these remote locations and from the South African continental shelf to assess genetic structure and population connectivity in S. lalandi and investigated life-history traits by comparing diet, age, growth and maturation among the three sites. The results suggest that yellowtail from South Africa and the two seamounts are genetically and phenotypically distinct. Rather than mere feeding oases, we postulate that these seamounts represent islands of breeding populations with site-specific adaptations.