Different plant-feeders, including insects and parasitic nematodes, can influence each other by triggering systemic changes in their shared host plants. In most cases however, the underlying mechanisms are unclear, and the consequences for plant fitness are not well understood. We studied the interaction between leaf feeding Manduca sexta caterpillars and root parasitic nematodes in Nicotiana attenuata. Simulated Manduca sexta attack increased the abundance of root parasitic nematodes in the field and facilitated Meloidogyne incognita reproduction in the glasshouse. Intact jasmonate biosynthesis was found to be required for both effects. Flower counts revealed that the jasmonate-dependent facilitation of nematode infestation following simulated leaf attack reduces the plant's reproductive potential to a greater degree than would be expected from the additive effects of the individual stresses. This work reveals that jasmonates mediate the interaction between a leaf herbivore and root parasitic nematodes and illustrates how plant-mediated interactions can alter a plant's reproductive potential. The selection pressure resulting from the demonstrated fitness effects is likely to influence the evolution of plant defense traits in nature.