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Pod borer <i>Helicoverpa armigera</i>, a polyphagus herbivorous pest, tremendously incurs crop damage in economically important crops. This necessitates the identification and utility of novel genes for the control of the herbivore. The present study deals with the characterization of a <i>flavonoid 3′5′ hydroxylase_2</i> (<i>F3′5′H_2</i>) from a pigeonpea wild relative <i>Cajanus platycarpus</i>, possessing a robust chemical resistance response to <i>H. armigera</i>. Though <i>F3′5′H_2</i> displayed a dynamic expression pattern in both <i>C. platycarpus</i> (Cp) and the cultivated pigeonpea, <i>Cajanus cajan (</i>Cc<i>)</i> during continued herbivory, <i>CpF3′5′H_2</i> showed a 4.6-fold increase vis a vis 3-fold in <i>CcF3′5′H_2</i>. Despite similar gene copy numbers in the two <i>Cajanus</i> spp., interesting genic and promoter sequence changes highlighted the stress responsiveness of <i>CpF3′5′H_2</i>. The relevance of <i>CpF3′5′H_2</i> in <i>H. armigera</i> resistance was further validated in <i>CpF3′5′H_2</i>-overexpressed transgenic tobacco based on reduced leaf damage and increased larval mortality through an in vitro bioassay. As exciting maiden clues, <i>CpF3′5′H_2</i> deterred herbivory in transgenic tobacco by increasing total flavonoids, polyphenols and reactive oxygen species (ROS) scavenging capacity. To the best of our knowledge, this is a maiden attempt ascertaining the role of <i>F3′5′H_2</i> gene in the management of <i>H. armigera.</i> These interesting leads suggest the potential of this pivotal branch-point gene in biotic stress management programs.