Organisms that face behavioural challenges can use different types of information to guide their decisions. First, they can use the personal information they sample in their environment. Second, they can use the inadvertent social information provided by the behaviour of conspecifics or heterospecifics (i.e. public information). Currently, little is known about the interaction between genetic variation and the use of personal versus public information in natural populations. Here, we investigated whether a natural genetic polymorphism affects the use of personal versus public information in a spatial learning task in Drosophila melanogaster. We found that genetic variation at the foraging locus interacts with social context during spatial learning. While both allelic variants are able to use personal and public information to improve their navigation during 10 training trials, a probe trial revealed that individuals carrying the forR (rover) allele rely mainly on personal information, whereas individuals carrying the fors (sitter) allele either use or display more public information than rovers. Accordingly, transfer of social information is more important in groups of sitters than in groups of rovers. These results suggest that a positive feedback loop can occur between alleles promoting group living, such as fors, and the use and/or display of public information, ultimately providing the opportunity for the joint evolution of sociality and cultural traits.