SummaryBrown planthopper (BPH,Nilaparvata lugens), a highly destructive insect pest, poses a serious threat to rice (Oryza sativa) production worldwide. Jasmonates are key phytohormones that regulate plant defences against BPH; however, the molecular link between jasmonates and BPH responses in rice remains largely unknown. Here, we discovered a Poaceae‐specific metabolite, mixed‐linkage β‐1,3;1,4‐d‐glucan (MLG), which contributes to jasmonate‐mediated BPH resistance. MLG levels in rice significantly increased upon BPH attack. OverexpressingOsCslF6, which encodes a glucan synthase that catalyses MLG biosynthesis, significantly enhanced BPH resistance and cell wall thickness in vascular bundles, whereas knockout ofOsCslF6reduced BPH resistance and vascular wall thickness. OsMYC2, a master transcription factor of jasmonate signalling, directly controlled the upregulation ofOsCslF6in response to BPH feeding. The AT‐rich domain of theOsCslF6promoter varies in rice varieties from different locations and natural variants in this domain were associated with BPH resistance. MLG‐derived oligosaccharides bound to the plasma membrane‐anchored LECTIN RECEPTOR KINASE1 OsLecRK1 and modulated its activity. Thus, our findings suggest that the OsMYC2‐OsCslF6 module regulates pest resistance by modulating MLG production to enhance vascular wall thickness and OsLecRK1‐mediated defence signalling during rice‐BPH interactions.