Theory suggests that frequency‐dependent resource competition will disproportionately impact the most common phenotypes in a population. The resulting disruptive selection forms the driving force behind evolutionary models of niche diversification, character release, ecological sexual dimorphism, resource polymorphism, and sympatric speciation. However, there is little empirical support for the idea that intraspecific competition generates disruptive selection. This paper presents a test of this theory, using natural populations of the three‐spine stickleback, Gasterosteus aculeatus. Sticklebacks exhibit substantial individual specialization associated with phenotypic variation and so are likely to experience frequency‐dependent competition and hence disruptive selection. Using body size and relative gonad mass as indirect measures of potential fecundity and hence fitness, I show that an important aspect of trophic morphology, gill raker length, is subject to disruptive selection in one of two natural lake populations. To test whether this apparent disruptive selection could have been caused by competition, I manipulated population densities in pairs of large enclosures in each of five lakes. In each lake I removed fish from one enclosure and added them to the other to create paired low‐ and high‐population‐density treatments with natural phenotype distributions. Again using indirect measures of fitness, disruptive selection was consistently stronger in high‐density than low‐density enclosures. These results support long‐standing theoretical arguments that intraspecific competition drives disruptive selection and thus may be an important causal agent in the evolution of ecological variation.