The sexy-sperm hypothesis posits that polyandrous females derive an indirect fitness benefit from multi-male mating because they increase the probability their eggs are fertilized by males whose sperm have high fertilizing efficiency, which is assumed to be heritable and conferred on their sons. However, whether this process occurs is contentious because father-to-son heritability may be constrained by the genetic architecture underlying traits important in sperm competition within certain species. Previous empirical work has revealed such genetic constraints in the seed beetle, Callosobruchus maculatus, a model system in sperm competition studies in which female multi-male mating is ubiquitous. Using the seed beetle, I tested a critical prediction of the sexy-sperm hypothesis that polyandrous females produce sons that are on average more successful under sperm competition than sons from monandrous females. Contrary to the prediction of the sexy-sperm hypothesis, I found that sons from monandrous females had significantly higher relative paternity in competitive double matings. Moreover, post-hoc analyses revealed that these sons produced significantly larger ejaculates when second to mate, despite being smaller. This study is the first to provide empirical evidence for post-copulatory processes favoring monandrous sons and discusses potential explanations for the unexpected bias in paternity.