Maternal effects can significantly impact offspring performance. Provisioning of offspring with energy stores can quantitatively alter their growth rates, survivorship, and future fecundity, and influence population regulatory mechanisms. In this paper, we show that maternal effects can also qualitatively affect offspring reproduction (i.e. their mode of reproduction). The freshwater herbivore Daphnia pulex can change the amount of energy allocated between asexual and ephippial egg production. Our experiments on individuals, experiencing “step-up” or “step-down” food manipulations, reveal that offspring qualitatively shift their energy allocation away from asexual reproduction to ephippial egg production when there is a simple mismatch between maternal and offspring food environments. We show that the response is asymmetric with respect to changes in food level, ephippial egg production is higher with a greater mismatch between environments, and that the effect can be observed in dynamic experimental populations. These results point to a “generational memory” that could challenge our interpretation of field patterns and mechanisms influencing population dynamics in Daphnia–algal systems.