Root-knot nematodes (RKN) are major crop pathogens worldwide. Trichoderma genus fungi are recognized biocontrol agents and a direct activity of Trichoderma atroviride (Ta) against the RKN Meloidogyne javanica (Mj), in terms of 42% reduction of number of galls (NG), 60% of number of egg masses and 90% of number of adult nematodes inside the roots, has been observed in tomato grown under greenhouse conditions. An in vivo split-root designed experiment served to demonstrate that Ta induces systemic resistance towards Mj, without the need for the organisms to be in direct contact, and significantly reduces NG (20%) and adult nematodes inside tomato roots (87%). The first generation (F1) of Ta-primed tomato plants inherited resistance to RKN; although, the induction of defenses occurred through different mechanisms, and in varying degrees, depending on the Ta-Mj interaction. Plant growth promotion induced by Ta was inherited without compromising the level of resistance to Mj, as the progeny of Ta-primed plants displayed increased size and resistance to Mj without fitness costs. Gene expression results from the defense inductions in the offspring of Ta-primed plants, suggested that an auxin-induced reactive oxygen species production promoted by Ta may act as a major defense strategy during plant growth.