Significance Intergenerational epigenetic inheritance is usually considered to be of minor significance in mammals because the epigenome is reprogrammed twice between each generation. Yet whether this paradigm holds in nonmammalian organisms is largely unknown. Here, we show that epigenetic marks are transferred across generations in an invertebrate, the honey bee. We found that the epigenome is much more similar between fathers and daughters than between unrelated males and females of different generations within each colony. Epigenetic marks are not only conserved across generations, but also across somatic and germline tissues. Epigenetic reprogramming may thus be a mammalian-specific feature, suggesting a heightened capacity for epigenetic marks to influence evolutionary adaptation across the tree of life.