The study investigates the impact of benzoxazinoids (BXs), a class of defensive secondary metabolites produced by cereal roots, on plant-soil feedbacks. BXs alter root-associated fungal and bacterial communities, decrease plant growth, increase jasmonate signaling and plant defenses, and suppress herbivore performance in the next generation. The breakdown product of BXs, 6-methoxy-benzoxazolin-2-one (MBOA), is identified as the key molecule responsible for these effects. MBOA accumulates in the soil during the conditioning phase and acts indirectly by altering the root-associated microbiota. Sterilization and microbial profiling experiments confirm that MBOA triggers changes in the rhizosphere microbiota, which in turn affect plant performance and defense. The findings provide a mechanism for how plants influence the composition of the rhizosphere microbiota, plant performance, and plant-herbivore interactions.The study investigates the impact of benzoxazinoids (BXs), a class of defensive secondary metabolites produced by cereal roots, on plant-soil feedbacks. BXs alter root-associated fungal and bacterial communities, decrease plant growth, increase jasmonate signaling and plant defenses, and suppress herbivore performance in the next generation. The breakdown product of BXs, 6-methoxy-benzoxazolin-2-one (MBOA), is identified as the key molecule responsible for these effects. MBOA accumulates in the soil during the conditioning phase and acts indirectly by altering the root-associated microbiota. Sterilization and microbial profiling experiments confirm that MBOA triggers changes in the rhizosphere microbiota, which in turn affect plant performance and defense. The findings provide a mechanism for how plants influence the composition of the rhizosphere microbiota, plant performance, and plant-herbivore interactions.