Children born to older parents tend to have lower intelligence and are at higher risk for disorders such as schizophrenia and autism. Such observations of ageing damage being passed on from parents to offspring are not often considered within the evolutionary theory of ageing. Here, we show the 25% memory impairment in Drosophila melanogaster offspring solely dependent on the age of the parents and also passed on to the F2 generation. Furthermore, this parental age effect was not attributed to a generalized reduction in condition of the offspring but was specific to short-term memory. We also provide evidence implicating oxidative stress as a causal factor by showing that lines selected for resistance to oxidative stress did not display a memory impairment in offspring of old parents. The identification of the parental age-related memory impairment in a model system should stimulate integration between mechanistic studies of age-related mortality risk and functional studies of parental age effects on the fitness of future generations.