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Summary Lignin, a complex heterogenous polymer present in virtually all plant cell walls, plays a critical role in protecting plants from various stresses. However, little is known about how lignin modifications in sorghum will impact plant defense against sugarcane aphids (SCA), a key pest of sorghum.We utilized the sorghumbrown midrib(bmr) mutants, which are impaired in monolignol synthesis, to understand sorghum defense mechanisms against SCA. We found that loss ofBmr12function and overexpression (OE) ofBmr12provided enhanced resistance and susceptibility to SCA, respectively, as compared with wild‐type (WT; RTx430) plants.Monitoring of the aphid feeding behavior indicated that SCA spent more time in reaching the first sieve element phase onbmr12plants compared with RTx430 andBmr12‐OE plants. A combination of transcriptomic and metabolomic analyses revealed thatbmr12plants displayed altered auxin metabolism upon SCA infestation and specifically, elevated levels of auxin conjugate indole‐3‐acetic acid–aspartic acid (IAA–Asp) were observed inbmr12plants compared with RTx430 andBmr12‐OE plants. Furthermore, exogenous application of IAA–Asp restored resistance inBmr12‐OE plants, and artificial diet aphid feeding trial bioassays revealed that IAA–Asp is associated with enhanced resistance to SCA.Our findings highlight the molecular underpinnings that contribute to sorghumbmr12‐mediated resistance to SCA.