1. Herbivory-induced changes in plant resistance and tolerance traits can mediate the interaction between spatially and temporally separated above- and belowground herbivores. However, it is unknown how long the impact of transient herbivory events last or if legacy effects can be detected systemically in the plant and across plant generations. 2. Here, we studied the impact of transient aboveground herbivory by the specialist caterpillar Manduca sexta on the plant traits of wild tobacco Nicotiana attenuata and the consequences for belowground root-knot nematodes Meloidogyne incognita in short-term, long-term, and transgenerational experiments. 3. In the short- and long-term experiments, above- and belowground herbivory had significant, albeit independent, impacts on key plant traits such as plant biomass, nutrient content, and secondary metabolites. In addition, herbivory influenced fitness parameters such as seed yield and quality. In the long-term and transgenerational experiments, transient aboveground herbivory had facilitating effects on nematodes, irrespective of any treatments of the parental plants. We found evidence for transgenerational legacy effects of both above- and belowground herbivory on the resistance of progeny plants against aboveground herbivores. Additionally, belowground herbivory in the parental generation increased the root biomass of progeny plants. 4. Synthesis. Our results suggest that herbivory may have a long-term impact on plant fitness by improving the performance of progeny plants challenged by above- and belowground herbivory.