Organisms are increasingly facing multiple stressors, which can simultaneously interact to cause unpredictable impacts compared to a single stressor alone. Recent evidence suggests that phenotypic plasticity can allow for rapid responses to altered environments, including biotic and abiotic stressors, both within a generation and across generations (transgenerational plasticity). Parents can potentially ‘prime’ their offspring to better cope with similar stressors, or, alternatively, might produce offspring that are less fit because of energetic constraints. At present, it remains unclear exactly how biotic and abiotic stressors jointly mediate the responses of transgenerational plasticity, and whether this plasticity is adaptive. Here we test the effects of biotic and abiotic environmental changes on within- and trans-generational plasticity using a Daphnia-Metschnikowia zooplankton-fungal parasite system. By exposing parents and their offspring consecutively to the single and combined effects of temperature elevation and parasite infection, we showed that transgenerational plasticity induced by temperature and parasite stress influenced host fecundity and lifespan; offspring of mothers that were exposed to one of the stressors were better able to tolerate temperature elevation, compared to offspring of mothers that were exposed to neither or both stressors. Yet the negative effects caused by parasite infection were much stronger, and this greater reduction in host fitness was not mitigated by transgenerational plasticity. We also showed that temperature elevation led to a lower average immune response, but the nature of its relationship with fecundity reversed under elevated temperatures; this suggests that parents that were exposed to parasites can potentially prime their offspring to respond to the joint stressors of both temperature elevation and parasite infection. Together, our results highlight the need to address questions at the interface of multiple stressors and transgenerational plasticity, and the importance of considering multiple fitness-associated traits when evaluating the adaptive value of transgenerational plasticity under changing environments.