Demographic processes can substantially affect a species’ response to changing ecological conditions, necessitating the combined consideration of genetic responses to environmental variables and neutral genetic variation. Using a seascape genomics approach combined with population demographic modelling, we explored the interplay of demographic and environmental factors that shaped the current population structure in Indo-Pacific bottlenose dolphins (Tursiops aduncus) along most of the western Australian coastline. We combined large-scale environmental data gathered via remote sensing with RADseq genomic data from 138 individuals at 19 sampling sites. Using population genetic and outlier detection anaylses, we identified three distinct genetic clusters, coinciding with tropical, subtropical and temperate provincial bioregions. In contrast to previous studies, our demographic models indicated that populations occupying the paleo-shoreline split into two demographically independent lineages before the last glacial maximum (LGM). A subsequent split after the LGM at 8.5 kya gave rise to the Shark Bay population, thereby creating the three currently observed clusters. Although multi-locus heterozygosity declined from north to south, dolphins from the southernmost cluster inhabiting temperate waters had higher heterozygosity in potentially adaptive loci, compared to dolphins from subtropical and tropical waters. These findings suggest ongoing adaptation to cold temperate waters in the southernmost cluster, possibly linked to distinct selective pressures between the different bioregions. Our study demonstrated that in the marine realm, without apparent physical boundaries, only a combined approach can fully elucidate the intricate environmental and genetic interactions shaping the evolutionary trajectory of marine mammals.