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Management of pod borer, <i>Helicoverpa armigera</i> in pigeonpea (<i>Cajanus cajan</i> L.), an important legume crop, has been a pertinent endeavor globally. As with other crops, wild relatives of pigeonpea are bestowed with various resistance traits that include the ability to deter the <i>H. armigera.</i> Understanding the molecular basis of pod borer resistance could provide useful leads for the management of this notorious herbivore. Earlier studies by our group in deciphering the resistance response to herbivory through multiomics approaches in the pigeonpea wild relative, <i>Cajanus platycarpus,</i> divulged the involvement of the flavonoid biosynthesis pathway, speculating an active chemical response of the wild relative to herbivory. The present study is a deeper understanding of the chemical basis of pod borer (<i>H. armigera</i>) resistance in, <i>C. platycarpus,</i> with focus on the flavonoid biosynthesis pathway. To substantiate, quantification of transcripts in <i>H. armigera</i>-challenged <i>C. platycarpus</i> (8 h, 24 h, 48 h, 96 h) showed dynamic upregulation (up to 11-fold) of pivotal pathway genes such as chalcone synthase, dihydroflavonol-4-reductase, flavonoid-3′5′-hydroxylase, flavonol synthase, leucoanthocyanidin reductase, and anthocyanidin synthase. Targeted LC-MS analyses demonstrated a concomitant increase (up to 4-fold) in naringenin, kaempferol, quercetin, delphinidin, cyanidin, epigallocatechin, and epicatechin-3-gallate. Interestingly, <i>H. armigera</i> diet overlaid with the over-produced flavonoids (100 ppm) showed deleterious effects on growth leading to a prolonged larval period demonstrating noteworthy coherence between over-accumulation of pathway transcripts/metabolites. The study depicts novel evidence for the directed metabolic reprogramming of the flavonoid biosynthesis pathway in the wild relative to pod borer; plant metabolic potential is worth exploiting for pest management.