We analyzed a transcriptome generated from four developmental stages of Heortia vitessoides Moore (Lepidoptera: Crambidae), a defoliator of the agarwood tree, Aquilaria sinensis (Lour.) Gilg (Thymelaeaceae). A total of 110.53 Mb clean reads were produced, and de novo assembled into 42,946 unigenes of an average length of 1,059 base pairs (bp). Among these unigenes, 22,106 (51.47%) showed significant similarity (E-value <10^–5) to known proteins in the National Center for Biotechnology Information (NCBI) nonredundant database. Gene ontology (GO), eukaryotic ortholog groups (KOG), and Kyoto Encyclopedia of Genes and Genomes (KEGG) analyses were used to classify the functionality of unigenes. Moreover, 46 putative cytochrome P450 (CYP) monooxygenase genes were identified from this dataset. These CYP genes were classified into four clans consisting of 22 families and 34 subfamilies. The expression profiles of genes belonging to CYP4 and CYP6 families and exposed to half the lethal concentrations (LC₅₀) of chlorantraniliprole and beta-cypermethrin were determined by real-time reverse transcription-quantitative PCR (RT-qPCR). The results showed that the transcription levels of eight (CYP4M39, CYP6AB49, CYP6AB53, CYP6AB61, CYP6AE17, CYP6AW1, CYP6BD6, CYP6CV1) and five (CYP6AB10, CYP6AB53, CYP6AE12, CYP6AE17, CYP6BD6) genes significantly increased in the fourth-instar larvae following exposure to the insecticides chlorantraniliprole and beta-cypermethrin, respectively. Therefore, these genes are potential candidates involved in the detoxification of these two insecticides. Further studies utilizing the RNA interference approach are required to enhance our understanding of the functionality of these genes in this forest pest.