Online enhancements: appendixes, supplemental PDF. Dryad data: http://dx.doi.org/10.5061/dryad.bc94c.abstract: The evolution of male traits that inflict direct harm on females during mating interactions can result in a so-called tragedy of the commons, where selfish male strategies depress population viability. This tragedy of the commons can be magnified by intralocus sexual conflict (IaSC) whenever alleles that reduce fecundity when expressed in females spread in the population because of their benefits in males. We evaluated this prediction by detailed phenotyping of 73 isofemale lines of the seed beetle Callosobruchus maculatus. We quantified genetic variation in life history and morphology, as well as associated covariance in male and female adult reproductive success. In parallel, we created replicated artificial populations of each line and measured their productivity. Genetic constraints limited independent trait expression in the sexes, and we identified several instances of sexually antagonistic covariance between traits and fitness, signifying IaSC. Population productivity was strongly positively correlated to female adult reproductive success but uncorrelated with male reproductive success. Moreover, male (female) phenotypic optima for several traits under sexually antagonistic selection were exhibited by the genotypes with the lowest (highest) population productivity. Our study forms a direct link between individuallevel sex-specific selection and population demography and places lifehistory traits at the epicenter of these dynamics.