The importance of root herbivory is increasingly recognized in ecological studies, and the effects of root herbivory on plant growth, chemistry, and performance of aboveground herbivores have been relatively well studied. However, how belowground herbivory by root feeding insects affects aboveground parasitoid development is largely unknown. In this study, we examined the effects of root herbivory by wireworms (Agriotes lineatus) on the expression of primary and secondary compounds in the leaves and roots of ragwort (Jacobaea vulgaris). We also studied the effects of root herbivory on the performance of a generalist aboveground herbivore, Mamestra brassicae and its parasitoid Microplitis mediator. In contrast to what most other studies have reported, root herbivory in J. vulgaris had a strong negative effect on the total concentration of pyrrolizidine alkaloids (PAs) in shoot tissues. The composition of PAs in the shoots also changed after root herbivory. In particular, the concentration of less toxic N-oxide PAs decreased. There was no significant effect of root herbivory on PA composition and concentration in the roots. Although the concentration of PA in the leaves decreased, M. brassicae tended to grow slower on the plants exposed to root herbivory. Parasitoid performance was not affected by root herbivory, but parasitoids developed faster when the concentration of jacobine-type PAs in the foliage was higher. These results point at a putative role of individual PAs in multitrophic interactions and emphasize that generalizations about aboveground-belowground effects should be made with great caution.