Green tea catechins are major plant defense compounds against herbivores, yet certain spider mite populations have evolved to use tea Camellia sinensis as a host plant. While the extreme generalist Tetranychus urticae (two-spotted spider mite; TSSM) has never been reported as a tea pest, some T. kanzawai (Kanzawa spider mite; KSM) populations thrive on tea. This variation provides a powerful system to dissect the molecular mechanisms underlying host plant adaptation. This study aimed to characterize how catechins affect mite behavior and performance, and to identify the gene(s) responsible for catechin adaptation in a KSM population collected from a tea farm. We used three mite populations: tea-adapted KSM from a tea farm in Japan, tea non-adapted KSM from an apple orchard in Japan, and laboratory TSSM. We assessed mite performance on tea and kidney bean leaves (5 runs). We evaluated the toxicity (3 to 5 runs), contact irritancy (10 or 11 runs), and antifeedancy (3 to 7 runs) of catechins (epigallocatechin gallate, epigallocatechin, epicatechin gallate, and epicatechin). We conducted comparative transcriptomics (2 runs) and proteomics (3 runs) on all three populations fed on tea or kidney bean leaves. We validated candidate gene function by RNAi-mediated silencing (5 runs) and measured enzymatic activities toward individual catechins using recombinant proteins (3 runs). Green tea catechins exerted complex defensive effects (toxicity, contact irritancy, and antifeedancy) against TSSM and non-adapted KSM, whereas tea-adapted KSM were largely insensitive to all three modes of action. Integrated transcriptomics and proteomics identified TkDOG15, an intradiol ring-cleavage dioxygenase horizontally transferred from fungi, as the only gene upregulated at both mRNA and protein levels specifically in tea-adapted KSM feeding on tea. RNAi-mediated silencing of TkDOG15 significantly reduced survival of tea- adapted KSM on tea leaves. Biochemical characterization revealed that two amino acid substitutions (Q127A and T203A) in TkDOG15, compared to TuDOG15, confer enhanced enzymatic activity toward green tea catechins. The amino acid sequence of TkDOG15 was identical between tea-adapted and non-adapted KSM, indicating that intraspecific differences arise solely from transcriptional upregulation. These findings support a two-step adaptation model in which structural refinement of DOG15 equips KSM over TSSM to use tea as a host plant, and its inducible expression enables efficient detoxification of catechins. This study provides the first experimental evidence linking a horizontally transferred DOG to host plant specialization, with implications for the plant- herbivore arms race and pest mite management in tea cultivation.