<!--StartFragment -->Plants mediate interactions between herbivores that attack simultaneously or sequentially above-groun (AG) and below-groun (BG) parts. Local and systemic induction of hormonal pathways and the concomitant increase in defense metabolites underlie these AG-BG interactions. However, the main plant-mediated mechanisms driving these reciprocal interactions via local and systemic induced responses remain ambiguous. I investigated the impact of root infection by root-knot nematode (RKN) Meloidogyne incognita at different stages of its infection cycle, on tomato leaf defense responses induced by Spodoptera exigua (caterpillar) and Macrosiphum euphorbiae (aphid). Also, I analyzed the reverse impact of caterpillar and aphid feeding on root responses induced by RKN. I measured changes in phytohormone and metabolic profiles in roots and leaves of plants exposed to a combination of RKN and one AG herbivore, at three stages of RKN infection; invasion, galling, and reproduction. I found that root infection by RKN enhanced caterpillar performance only at the galling stage, but no effect on the aphid regardless of infection cycle stage. Next, I analyzed for mechanisms driving the observed effects. RKN broadly enhanced responses related to jasmonic acid (JA) pathway and metabolites triggered by caterpillar in leaves, throughout the infection cycle. For the aphid, there was no effect on phytohormone, but metabolites increased in leaves. The reciprocal effects of AG feeding on root induced responses to RKN, showed that caterpillar feeding interfered with JA related responses at the reproduction stage while aphid did not alter root responses induced by RKN regardless of infection stage. These results show that RKN root infection cycle is an important factor influencing the reciprocal interaction with different AG insect herbivores. These results generate a better understanding of the mechanisms underlying frequent RKN-insect herbivore interactions in natural and agricultural ecosystems.