In insects, the transcription factor cap ‘n’ collar isoform C (CncC) plays a critical role in the regulation of multiple genes involved in insecticide detoxification. Knockdown of CncC genes leads to increased susceptibility to different types of insecticides in several insect species. However, the CncC gene has not yet been fully characterized in the black cutworm Agrotis ipsilon, a notorious insect pest that causes severe damage to field crops. In this study, the CncC gene (designated AiCncC) was identified from A. ipsilon. Exposure to a median lethal concentration (LC50) of chlorantraniliprole (CAP) or phoxim (PHO) strongly increased the expression of AiCncC. Silencing of AiCncC by RNA interference significantly increased the susceptibility of A. ipsilon larvae to both insecticides. Moreover, CncC/Maf binding sites were predicted in the putative promoters of two glutathione S-transferase (GST) genes (AiGSTe1 and AiGSTu1) involved in the detoxification of CAP and PHO. The transcription levels of AiGSTe1 and AiGSTu1 were dramatically decreased by silencing AiCncC. These findings indicate that AiCncC is associated with CAP and PHO susceptibility through the regulation of GST genes.