Reproductive conflict between the sexes is thought to be a key force in the evolution of many reproductive characters, but persuasive evidence for its significance is still scarce. The spectacular evolution of male genitalia that impose physical injury on females during mating has often been suggested to be a product of sexually antagonistic coevolution, but our understanding of these extraordinary adaptations is very limited, and there are no direct data addressing their evolutionary elaboration. We show that more spiny male genitalia causes more harm to females during copulation and provide comparative evidence for the correlated evolution between these antagonistic adaptations in males and a female counteradaptation (the amount of connective tissue in the copulatory duct) in a group of insects. By combining comparative and experimental methods, we demonstrate that imbalance of relative armament of the sexes affects evolution of the economics of reproduction: as males evolve genitalia that are more harmful relative to the level of female counteradaptation, costs associated with mating for females increase and population fitness is depressed. Our results unveil a coevolutionary arms race between the sexes and are consistent with a proposed link between sexual conflict, species' viability, and the risk of extinction.