Lepidoptera produce two kinds of sperm, eusperm, which are conventional nucleated spermatozoa, and parasperm, which lack nuclei and are usually smaller. Both travel in the female to the sperm storage organ, the spermatheca, but there the parasperm become inactive or disappear without taking any direct role in fertilization of the eggs. There are widespread accounts in the literature of an excess of parasperm over eusperm, though relatively few actual counts, and those counts are from various locations in the lifetime of the sperm: from testes, seminal vesicles, ejaculates, or spermathecae. With phylogenetic comparisons in mind, we counted sperm in the final sperm storage organs of males, the seminal vesicles (ductus ejaculatorius duplex), to explore the prevalence of these two types of sperm over a wide range of species and sizes. We found parasperm in all species, including the most phylogenetically basal (non-ditrysian) ones, and a preponderance of parasperm over eusperm in almost all, including a majority of the smaller species with small total numbers of sperm. Total sperm number of both types increased with wingspan (our proxy for size) as did the ratio of parasperm to eusperm. The ubiquity of parasperm and their preponderance even in very small species indicates an important role in lepidopteran reproduction. Further, the large numbers of both sperm types in larger species of Lepidoptera, apparently vastly more than are needed to fertilize eggs, suggests a role in sperm competition.