Cyclic parthenogens alternate asexual reproduction with periodic episodes of sexual reproduction. Sexually produced free-living forms are often their only way to survive unfavorable periods. When sexual reproduction requires the mating of two self-incompatible individuals, mating limitation may generate an Allee effect, which makes small populations particularly vulnerable to extinction; parthenogenetic reproduction can attenuate this effect. However, asexual reproduction likely trades off with sexual reproduction. To explore the evolutionary implications of such a trade-off, we included recurrent mating events associated with seasonal interruptions in a simple population dynamics model. Following an adaptive dynamics approach, we showed that positive density dependence associated with Allee effects in cyclic parthenogens promotes evolutionary divergence in the level of investment in asexual reproduction. Although polymorphism may be transient, morphs mostly investing into sexual reproduction may eventually exclude those predominantly reproducing in an asexual manner. Asexual morphs can be seen as making cooperative investments into the common pool of mates, while sexual morphs defect, survive better, and may eventually fix in the population. Our findings provide a novel hypothesis for the frequent coexistence of sexual and asexual lineages, notably in plant parasitic fungi.