Plants can respond to environmental cues that predict impending herbivory by priming appropriate defences; yet, we have limited knowledge about how priming cues that change plant defence phenotype, can also influence plant fitness. Here we show that volatiles induced by herbivore eggs—prior to any feeding damage—can prime defences in neighbouring plants. Working with both an annual, black mustard (Brassica nigra), and a perennial, Brussel sprouts (Brassica oleracea), we found that volatiles induced by the eggs of a specialist herbivore, the large cabbage white butterfly Pieris brassicae, elicited enhanced defence responses to subsequent herbivory that reduced herbivore performance. Interestingly, Brassica nigra plants exposed to oviposition-induced plant cues also showed significantly higher flower and seed numbers compared to non-exposed plants, indicating that priming cues can also influence plant fitness. These findings provide evidence for an unexplored role of plant-insect interactions to fitness benefits from insect-derived olfactory cues, even before actual herbivory is present.