Cajanus scarabaeoides (L.), Thouars, is the closest wild crop relative of cultivated pigeonpea, Cajanus cajan (L.), Millspaugh. This wild pigeonpea has several insect-resistance mechanisms, particularly to Helicoverpa armigera (Hübner). Estimated economic losses in the semi-arid tropics from H. armigera damage in pigeonpea are approximately two billion USD/year. Therefore, it is imperative to improve pest resistance in this crop. In this study, we investigated insect-resistance components in IBS 3471, a C. scarabaeoides accession, and explored the possibility of transferring resistance mechanism/s to cultivated pigeonpea. A detached leaf bioassay revealed that IBS 3471 has more effective antibiosis and antixenosis resistance mechanisms against H. armigera compared to the susceptible C. cajan variety, ICPL 87. To further investigate the antibiosis resistance mechanism, we fed H. armigera larvae a heated and non-heated artificial diet supplemented with lyophilised IBS 3471 leaf powder. Incorporation of IBS 3471 leaf powder inhibited H. armigera larval weight and delayed larval development compared to larvae reared on diet supplemented with ICPL 87 leaf powder. The putative insect-resistance compounds in C. scarabaeoides were heat-labile. Proteomic analysis revealed higher levels of potential insecticidal proteins, namely lectin and cysteine proteinase inhibitor, in wild pigeonpea compared to the cultivated variety. Nutritional analysis and interspecific hybridisation experiments also indicated that IBS 3471 is a potential candidate for improvement of insect-resistance in pigeonpea. This study demonstrates that IBS 3471 has multiple resistance mechanisms against H. armigera, and they are transferable to cultivated pigeonpea.