An individual’s phenotype can be altered by direct contact with its present environment but also by environmental features experienced by previous generations, i.e. parental or grandparental effects. However, the strength and direction of these transgenerational effects may be highly variable according to the ecological conditions experienced by ancestral generations. Here we performed a reciprocal split-brood experiment to compare transgenerational responses to the threat of ultraviolet radiation (UVR) in the zooplankter Daphnia magna, which had, or had not, been exposed to UVR for more than 150 generations, respectively. We found that the environment at which parents and grandparents were reared significantly influenced both behavior and life-history traits of their descendants. However, such transgenerational responses differed between D. magna individuals with contrasting ancestral stress history, that is, when exposed to UVR previously unexposed individuals rapidly changed their behavior and life-history traits, whereas individuals previously exposed to UVR showed less pronounced response when the UVR threat level relaxed. Hence, we here demonstrate an asymmetric transgenerational plasticity in response to UVR threat. The findings advance our understanding on the evolutionary ecology of such transgenerational effects and their potential role in response to changes in the local environment.