Sperm competition and cryptic female choice profoundly affect sperm morphology, producing diversity within both species and individuals. One type of within‐individual sperm variation is sperm heteromorphism, in which each male produces two or more distinct types of sperm simultaneously, only one of which is typically fertile (the ‘eusperm’). The adaptive significance of nonfertile ‘parasperm’ types is poorly understood, although numerous sperm‐heteromorphic species are known from many disparate taxa. This paper examines in detail two female‐centred hypotheses for the evolution and maintenance of this unconventional sperm production strategy. First, we use game theoretical models to establish that parasperm may function to protect eusperm from female‐generated spermicide, and to elucidate the predictions of this idea. Second, we expand on the relatively undeveloped idea that parasperm are used by females as a criterion for cryptic female choice, and discuss the predictions generated by this idea compared to other hypotheses proposed to explain sperm heteromorphism. We critically evaluate both hypotheses, suggest ways in which they could be tested, and propose taxa in which they could be important.