Trait evolution via sexual selection has traditionally been viewed as isolated from life–history constraints. Recent theoretical treatments, however, predict that costly sexually selected characters should be mediated by the same allocational trade–offs that apply to more conventional aspects of reproductive investment. Participation in risky competitive behaviours, for example male–male combat, should therefore increase as the opportunity for future reproduction declines. However, the demonstration of such trade–offs has proven to be elusive due to concomitant age–based variation in the physical determinants of fighting ‘ability’. Here, I exploit the unique nature of a butterfly contest system to provide compelling evidence for lifetime partitioning of risky and aggressive sexually selected behaviours. I show that male Hypolimnas bolina become more willing to persist in contests over mating territories, and more generally accepting of injury risks, as they age. Contest persistence in this species is not mediated simply by physical condition, and I experimentally isolate the effect of ageing per se from resource ownership and previous contest experience. These results demonstrate how sexually selected behaviours can be ultimately mediated by a shifting trade–off between contemporary reproductive effort and future opportunities.