The dispersal and migration of organisms have resulted in the colonisation of nearly every possible habitat and ultimately the extraordinary diversity of life. Animal dispersal tendencies are commonly heterogeneous (e.g. long vs. short) and non-random suggesting that phenotypic and genotypic variability between individuals can contribute to population-level heterogeneity in dispersal. Using laboratory and field experiments, we demonstrate that natural allelic variation in a gene underlying a foraging polymorphism in larval fruit flies (for), also influences their dispersal tendencies as adults. Rover flies (forR; higher foraging activity) have consistently greater dispersal tendencies and are more likely to disperse longer distances than sitter flies (fors; lower foraging activity). Increasing for expression in the brain and nervous system increases dispersal in sitter flies. Our study supports the notion that variation in dispersal can be driven by intrinsic variation in food-dependent search behaviours and confirms that single gene pleiotropic effects can contribute to population-level heterogeneity in dispersal.