The identification of genetically distinct populations is central to the management and conservation of wild populations. Whole-genome-sequencing allows for high-resolution assessment of genetic structure, demographic connectivity and the impacts of selection acting on different parts of the genome. Here, we utilise population genomics to investigate the genetic structure of the Australasian snapper or Tāmure (Chrysophrys auratus), an ecologically, economically, and culturally important (taonga) marine fish. We analysed over four million high-quality SNPs obtained by whole-genome sequencing from 382 individuals collected across its New Zealand range. We identified two genetic clusters (an eastern and western cluster) with genetic disjunctions around on either side of the North Island of New Zealand. These genetic clusters do not match the current fisheries management areas. Pairwise-F_ST and ADMIXTURE analyses showed the presence of directional gene flow occurring at both genetic disjunctions from the East to the West cluster. We hypothesize that major ocean currents are limiting the dispersal of snapper at these genetic disjunctions. The heterogeneous coastal environment is also likely driving evolutionary change. A genome scan identified four significantly divergent genomic regions between genetic clusters. A diverse pattern of genetic variation in these regions implies that different evolutionary processes drive local adaptation in these clusters. Identification of candidate genes in these regions also provides a tentative connection to which traits may be under selection. Our results provide novel insights into New Zealand’s coastal environment influences evolutionary processes, and valuable information for effective management of the snapper fisheries.