Oviposition by Spodoptera exigua on Nicotiana attenuata primes plant defence against its larvae that consequently suffer reduced performance. To reveal whether this is a general response of tobacco to insect oviposition or species-specific, we investigated whether also Manduca sexta oviposition primes N.attenuata's anti-herbivore defence. The plant response to M.sexta and S.exigua oviposition overlapped in the egg-primed feeding-induced production of the phenylpropanoid caffeoylputrescine. While M.sexta larvae were unaffected in their performance, they showed a novel response to the oviposition-mediated plant changes: a reduced antimicrobial activity in their haemolymph. In a cross-resistance experiment, S.exigua larvae suffered reduced performance on M.sexta-oviposited plants like they did on S.exigua-oviposited plants. The M.sexta oviposition-mediated plant effects on the S.exigua larval performance and on M.sexta larval immunity required expression of the NaMyb8 transcription factor that is governing biosynthesis of phenylpropanoids such as caffeoylputrescine. Thus, NaMyb8-dependent defence traits mediate the effects that oviposition by both lepidopteran species exerts on the plant's anti-herbivore defence. These results suggest that oviposition by lepidopteran species on N.attenuata leaves may generally prime the feeding-induced production of certain plant defence compounds but that different herbivore species show different susceptibility to egg-primed plant effects. Insects often lay their eggs on the plant that their larvae feed from. We demonstrated that oviposition by different lepidopteran herbivores on a wild tobacco primes the feeding-induced production of similar defensive traits. This plant response impairs the larval development of a generalist herbivore and the larval immune status of a specialist. These results highlight both the generality and the specificity by which insect oviposition on a host plant can affect plant-insect interactions.