Socially learned behaviours leading to genetic population structure have rarely been described outside humans. Here, we provide evidence of fine-scale genetic structure that has probably arisen based on socially transmitted behaviours in bottlenose dolphins (Tursiops sp.) in western Shark Bay, Western Australia. We argue that vertical social transmission in different habitats has led to significant geographical genetic structure of mitochondrial DNA (mtDNA) haplotypes. Dolphins with mtDNA haplotypes E or F are found predominantly in deep (more than 10 m) channel habitat, while dolphins with a third haplotype (H) are found predominantly in shallow habitat (less than 10 m), indicating a strong haplotype-habitat correlation. Some dolphins in the deep habitat engage in a foraging strategy using tools. These 'sponging' dolphins are members of one matriline, carrying haplotype E. This pattern is consistent with what had been demonstrated previously at another research site in Shark Bay, where vertical social transmission of sponging had been shown using multiple lines of evidence. Using an individual-based model, we found support that in western Shark Bay, socially transmitted specializations may have led to the observed genetic structure. The reported genetic structure appears to present an example of cultural hitchhiking of mtDNA haplotypes on socially transmitted foraging strategies, suggesting that, as in humans, genetic structure can be shaped through cultural transmission.