Male genitalia often show remarkable differences among related species in size, shape and complexity. Across poeciliid fishes, the elongated fin (gonopodium) that males use to inseminate females ranges from 18 to 53% of body length. Relative genital size therefore varies greatly among species. In contrast, there is often tight within-species allometric scaling, which suggests strong selection against genital–body size combinations that deviate from a species’ natural line of allometry. We tested this constraint by artificially selecting on the allometric intercept, creating lines of males with relatively longer or shorter gonopodia than occur naturally for a given body size in mosquitofish, Gambusia holbrooki. We show that relative genital length is heritable and diverged 7.6–8.9% between our up-selected and down-selected lines, with correlated changes in body shape. However, deviation from the natural line of allometry does not affect male success in assays of attractiveness, swimming performance and, crucially, reproductive success (paternity).