The evolution of a new reproductive strategy is expected to be reflected in an organism's genome and impact mating-related traits. Several species of Caenorhabditis nematodes have evolved the ability to self-fertilize from their outcrossing ancestors. Comparisons of species with different reproductive strategies may therefore reveal consequences of transition to self-fertilization. We compared chromosome-scale genome assemblies for the outcrossing nematode Caenorhabditis nigoni and its recently self-fertile sister species, C. briggsae. C. nigoni genome resembles that of outcrossing relatives but encodes 31% more protein-coding genes than C. briggsae. C. nigoni genes lacking C. briggsae orthologs were disproportionately small and male-biased in expression, including the male secreted short (mss) gene family that encodes sperm surface glycoproteins conserved only in outcrossing species. Sperm of mss-null males of an outcrossing species failed to compete with those of wild-type males, despite having normal fertility in non-competitive situations. Restoration of mss to C. briggsae males was sufficient to enhance sperm competitiveness. These results reveal the pervasive influence of sex on genome content that can be used to identify sperm competition factors. Further I found the fitness of mss+ genotype was influenced by mating system and population subdivision. Specifically, mss+ is sufficient to increase male frequency and depress population growth in genetically homogenous androdioecious populations. Using experimental evolution, I demonstrated that when mss+ and mss-null (i.e. wild-type) genotypes compete, mss+ is positively selected in both mixed-mating and strictly outcrossing situations, though more strongly in the latter. I suggest that the lack of inbreeding depression and the strong subdivision thought to characterize natural Caenorhabditis populations impose selection on sex ratio that makes loss of mss adaptive in self-fertile species.