ABSTRACT Mungbean [ Vigna radiata (L.) Wilczek], an important leguminous crop, is grown on more than six million hectares worldwide. However, mungbean is very susceptible to the common leaf‐feeding cutworm ( Spodoptera litura ), and its defence mechanism against S. litura is not fully understood. By integrating an ‘omic’ approach and comparing the results between the resistant wild accession (CQ3112) and susceptible cultivar (Crystal) after S. litura attacks, this study identified the key defensive regulatory genes and bioactive metabolites involved in resistance to S. litura . The transcriptomic results demonstrated that VrMYC2 , VrAOC , VrGH3 and VrPPO are involved in defence responses associated with jasmonic acid (JA) signalling, and VrUGT84A24 , VrIOMT and VrEBOS , involved in the terpenoid and flavonoid biosynthesis, are up‐regulated in responses to S. litura attacks. The metabolomic results further confirmed that JA, glucosylated kaempferol and ( E )‐β‐ocimene are accumulated in CQ3112 accession, supporting defence response to S. litura infestation. Moreover, feeding S. litura larvae with kaempferol‐7‐O‐glucoside (K7G), a non‐volatile metabolite identified in this study, showed S. litura growth and mortality reductions. Taken together, this study provides solid evidence that K7G functions as an insecticidal compound to control S. litura attacks. Also, the genes involved in defence against S. litura could provide genetic information for the improvement of mungbean breeding programmes.