Environmental conditions can shape genetic and morphological divergence. Release of new habitats during historical environmental changes was a major driver of evolutionary diversification. Here, forces shaping population structure and ecotype differentiation (‘pelagic’ and ‘coastal’) of bottlenose dolphins in the North-east Atlantic were investigated using complementary evolutionary and ecological approaches. Inference of population demographic history using approximate Bayesian computation indicated that coastal populations were likely founded by the Atlantic pelagic population after the Last Glacial Maxima probably as a result of newly available coastal ecological niches. Pelagic dolphins from the Atlantic and the Mediterranean Sea likely diverged during a period of high productivity in the Mediterranean Sea. Genetic differentiation between coastal and pelagic ecotypes may be maintained by niche specializations, as indicated by stable isotope and stomach content analyses, and social behaviour. The two ecotypes were only weakly morphologically segregated in contrast to other parts of the World Ocean. This may be linked to weak contrasts between coastal and pelagic habitats and/or a relatively recent divergence. We suggest that ecological opportunity to specialize is a major driver of genetic and morphological divergence. Combining genetic, ecological and morphological approaches is essential to understanding the population structure of mobile and cryptic species.