The tea plant (Camellia sinensis) is a unique beverage crop worldwide, but its yield and quality are adversely affected by Toxoptera aurantii. However, the response mechanisms of tea plants to T. aurantii stress remain poorly known. Herein, we present the life table of T. aurantii on resistant (W016) and susceptible (HJY) tea cultivars, demonstrating that the fitness of T. aurantii on W016 was lower than that on HJY. Integrated metabolic and transcriptomic analyses revealed that T. aurantii feeding activated pathways associated with phenylpropanoid biosynthesis, plant hormone signal transduction, and ATP-binding cassette (ABC) transporters. Notably, T. aurantii feeding significantly upregulated the levels of brassinolide and p-coumaryl alcohol in W016 but not in HJY. Furthermore, in vitro enzymatic assays indicated that C. sinensis cinnamyl alcohol dehydrogenase (CsCAD1) catalyzes the formation of p-coumaryl alcohol participation in lignin synthesis. Our findings highlight the role of brassinolide-mediated lignin biosynthesis of the tea plant in response to T. aurantii feeding.