Comparative studies show that variation in sperm morphometry across taxa is associated with the environment in which sperm function, and the species' mating pattern dictating the risk of sperm competition. Accordingly, sperm have evolved to function in a non-self environment (in contrast to somatic cells) and sperm morphometry is predicted to be optimized independently of the individual male producing them, but is the result of selective forces arising directly from the fertilization and competitive environment in which sperm will operate. Males within a population are therefore under stabilizing selection to produce an optimal distribution of sperm sizes. The nature of this distribution was explored using consistent techniques to measure detailed sperm morphometry for 10 species in a range of taxa from insects to humans. Although we expected variance in sperm morphometry to be optimized by every individual male through stabilizing selection at a population or species level, we found the exact opposite; for every species examined there was significant variation between individual males in the total lengths of the sperm they produced. A significant variation is reported between individual males for every species in the sizes of each sperm head, mid-piece and flagellum component. The between-male variation exists consistently in wild, domestic and human populations, subject to a wide range of levels of inbreeding. In gryllid crickets sperm length is shown to be male-specific and is repeatable between successive ejaculates. Between-female variation in ova size (data are presented for trout) is explainable by individual female fecundity optimization strategies; however, the adaptive significance of widespread between-individual variance in male gamete size is counter-intuitive and difficult to interpret, particularly as the limited evidence available shows that sperm morphometry is not condition-dependent or resource-constrained. The differences, however, do suggest negligible influences from haploid expression in the development of sperm morphometry – if haplotypic expression were manifested we would expect more profound variation within a male's sperm population (to reflect the inherent within-male variance in haplotypes derived from recombination) rather than the significant between-male differences we found that suggests the diploid control of spermatozoal phenotype.