Sperm cells provide crucial, if usually diminutive, ingredients to successful sexual reproduction as the source of centrioles and half the diploid genome. Despite this essential conserved function, sperm competition and coevolution with female traits has driven spectacular morphological change across the tree of life in these discrete cells. Here I characterize repeated instances of convergent evolution of sperm gigantism across the phylogeny of Caenorhabditis nematodes. Species at the extreme end of the 50-fold range of sperm-cell volumes have sperm capable of comprising ~5% of egg-cell volume, representing severe attenuation of the magnitude of anisogamy. We demonstrate that sperm size variation establishes early in spermatogenic development, by meiosis I during the formation of primary spermatocytes. We hypothesize that life history differences among species favored the evolution of alternative sperm competition strategies toward many small vs. fewer large sperm. A byproduct of the outcome of within-species sperm competition manifests during between-species mating errors, in which sperm from the ‘wrong’ species can invade distal gonad and somatic tissue of the mated female, leading to sterility and premature death. These gametic mismatches represent a form of post-mating pre-zygotic reproductive isolation, suggesting a potentially cryptic role of sexual selection by sperm competition in the speciation process.