Foraging differentiation within a species can contribute to restricted gene flow between ecologically different groups, promoting ecological speciation. Galapagos sea lions (Zalophus wollebaeki) show genetic and morphological divergence between the western and central archipelago, possibly as a result of an ecologically mediated contrast in the marine habitat. We use global positioning system (GPS) data, time-depth recordings (TDR), stable isotope and scat data to compare foraging habitat characteristics, diving behaviour and diet composition of Galapagos sea lions from a western and a central colony. We consider both juvenile and adult life stages to assess the potential role of ontogenetic shifts that can be crucial in shaping foraging behaviour and habitat choice for life. We found differences in foraging habitat use, foraging style and diet composition that aligned with genetic differentiation. These differences were consistent between juvenile and adult sea lions from the same colony, overriding age-specific behavioural differences. Our study contributes to an understanding of the complex interaction of ecological condition, plastic behavioural response and genetic make-up of interconnected populations.