Many marine species exhibit fine‐scale population structure despite high mobility and a lack of physical barriers to dispersal, but the evolutionary drivers of differentiation in these systems are generally poorly understood. Here we investigate the potential role of habitat transitions and seasonal prey distributions on the evolution of population structure in the Indo‐Pacific bottlenose dolphin, Tursiops aduncus, off South Africa’s coast, using double‐digest Restriction‐site Associated DNA sequencing (ddRADseq). Population structure was identified between the eastern and southern coasts and correlated with the habitat transition between the temperate Agulhas (southern) and subtropical Natal (eastern) Bioregions, suggesting differentiation driven by resource specialisations. Differentiation along the Natal coast was comparatively weak, but evident in some analyses and varied depending on whether the samples were collected during or outside the seasonal sardine (Sardinops sagax) run. This local abundance of prey could influence the ranging patterns and apparent genetic structure of T. aduncus. These findings have significant and transferable management implications, most importantly in terms of differentiating populations inhabiting distinct Bioregions and seasonal structural patterns within a region associated with the movement of prey resources.