Vast distances and permeable phylogeographic barriers characterize the open ocean, boosting gene flow and decreasing population structure and speciation of widely distributed and migratory species. However, many widely distributed species are formed by different populations throughout their distribution, evidencing our understanding of how the marine environment triggers population and species differentiation are insufficient. The sailfish is a circumtropical and highly migratory billfish that inhabits warm and productive areas. Despite its ecological and socioeconomic importance as a predator and fishery resource, the species is threatened by overfishing requiring innovative approaches to improve their management and conservation status. Thus, we presented an improved high-quality reference genome for the species and applied a seascape genomics approach to understand how marine environmental features may promote local adaptation and how it affects gene flow between populations. We delimit 2 populations between the Atlantic and Indo-Western Pacific oceans and detect 82 outlier loci correlated with sea surface temperature, salinity, oxygen, and chlorophyll concentrations. However, the most significant environmental feature that explains the differences between populations was isolation-by-distance. Sailfish populations were not inbred, although its genome-wide heterozygosity was lower for billfishes and marine fishes, evidencing the need to counteract overfishing effects. In addition, in a climate change scenario, management agencies must implement state-of-the-art sequencing methods, consider our findings in their management plans, and monitor genome-wide heterozygosity over time to improve sustainable fisheries and the long-term viability of its populations.