Bark beetles depend on detoxifying enzymes to counteract the defensive terpenoids produced by host trees. Insect ABC transporters play a critical role in the detoxification of insecticides and plant secondary metabolites. However, the specific functions of ABC genes in the metabolism of host allelochemicals remain unclear in D. armandi. In this study, we observed that verapamil significantly enhanced the mortality of host allelochemicals in beetles, indicating that ABC transporter genes are involved in the metabolism of monoterpenes by D. armandi. We then sequenced and characterized the full-length cDNAs of three ABCH subfamily genes (DaABCH1–DaABCH3) from D. armandi. Spatiotemporal expression profiling revealed that all three genes were upregulated during developmental transitions (egg to larva and pupa to adult) and tissue-specific enrichment in detoxification-related organs (Malpighian tubules, fat body, and midgut). Additionally, DaABCH3 expression was detected in the hindgut and brain. Furthermore, DaABCH1 and DaABCH2 were significantly induced by treatment with α-pinene and limonene, whereas DaABCH3 was induced by β-pinene and limonene. Importantly, silencing DaABCH1 significantly increased mortality in adults fumigated with α-pinene and limonene. These results strongly suggest that DaABCH1 acts as a key regulator modulating D. armandi’s sensitivity to host plant allelochemicals. This finding provides a conceptual basis for developing novel control strategies against this economically significant forest pest.