Cadherin proteins bind Bacillus thuringiensis (Bt) toxins in lepidopteran midguts but their inherent function remains unclear. In pink bollworm, Pectinophora gossypiella, three recessive mutations in a cadherin gene (BtR) are tightly linked with resistance to Bt toxin Cry1Ac. Here we examined patterns of transcription of this gene and the association between cadherin genotype and sperm transfer in pink bollworm. Cadherin RNA was most abundant in larvae, but was also found in adults and embryos. In fourth instar larvae, cadherin RNA was most abundant in the gut, yet its presence in the testes indicates a potential role in sperm production. Previously, we found reduced first-male paternity in pink bollworm males homozygous for cadherin mutations conferring resistance to Bt, when a resistant and susceptible male competed for access to a female. However, the number of offspring sired by resistant and susceptible males was similar without competition. Male Lepidoptera produce both fertile eupyrene sperm and anucleate, non-fertile apyrene sperm, suggesting that apyrene sperm may contribute to male reproductive success when sperm competition occurs. Accordingly, we hypothesized that cadherin-based resistance to Bt entails fitness costs that reduce apyrene sperm transfer. To test this hypothesis, we compared apyrene and eupyrene sperm transfer in males from four strains of pink bollworm. Transfer of apyrene and eupyrene sperm was lower in homozygous resistant than in susceptible males. Furthermore, homozygous resistant males weighed less than susceptible males, which could have diminished sperm transfer by resistant males directly, or via a positive association between male weight, spermatophore weight and sperm transfer. While data suggest that cadherin mutations induced a recessive fitness cost affecting apyrene sperm transfer, these mutations also generated recessive costs that affected other traits and could have lowered first-male paternity.