Life history theory is concerned with the costs of survival, growth and reproduction under different ecological conditions and the allocation of resources to meet these costs. Typical approaches used to address these topics include manipulation of food resources, followed by measures of subsequent reproductive traits, and measures of the relationship between current and future reproductive investment. Rarely, however, do studies test for the interaction of past investment, present resource availability and future investment simultaneously. Here, we investigate this interaction in females of a sexual parasite–host system consisting of the hybridogenetic frog Rana esculenta (E) and one of its parental species Rana lessonae (L). We kept females from each of two groups (with or without previous reproduction) under two food treatments (low or high) and regularly recorded their growth as well as their body condition and hormone titres as measures of future reproductive condition. After keeping them in hibernation until the following spring, we exposed the females to males, recorded whether they spawned or not and related this response to their condition in the previous autumn. Past reproduction negatively affected growth during summer and condition during autumn which, in turn, reduced the following year’s reproductive output. These costs of previous reproduction were less pronounced under the high than under the low food treatment and lower in R. lessonae than in R. esculenta. Increasing food supply improved reproductive condition more in L than in E females. These species differences in reproductive costs and food requirements provide a mechanistic explanation for why E females skip annual reproduction almost twice as often as L females. Since R. esculenta is a sexual parasite that depends on R. lessonae for successful reproduction, these species-specific life history patterns not only affect individual fitness but also the spatial structure and temporal dynamics of mixed LE populations.