Most flowering plants must defend themselves against herbivores for survival and attract pollinators for reproduction. Although traits involved in plant defence and pollinator attraction are often localised in leaves and flowers, respectively, they will show a diffuse evolution if they share the same molecular machinery and regulatory networks. We performed RNA-sequencing to characterise and compare transcriptomic changes involved in herbivory-induced defences and flower development, in tomato leaves and flowers, respectively. We found that both the herbivory-induced responses and flower development involved alterations in jasmonic acid signalling, suppression of primary metabolism and reprogramming of secondary metabolism. We identified 411 genes that were involved in both processes, a number significantly higher than expected by chance. Genetic manipulation of key regulators of induced defences also led to the expression changes in the same genes in both leaves and flowers. Targeted metabolomic analysis showed that among closely related tomato species, jasmonic acid and α-tomatine are correlated in flower buds and herbivory-induced leaves. These findings suggest that herbivory-induced responses and flower development share a common molecular machinery and likely have coevolved in nature.