Conditioning the soil microbiome through plant–soil feedbacks suppresses an aboveground insect pest

Summary Soils and their microbiomes are now recognized as key components of plant health, but how to steer those microbiomes to obtain their beneficial functions is still unknown. Here, we assess whether plant–soil feedbacks can be applied in a crop system to shape soil microbiomes that suppress herbivorous insects in above‐ground tissues. We used four grass and four forb species to condition living soil. Then we inoculated those soil microbiomes into sterilized soil and grew chrysanthemum as a focal plant. We evaluated the soil microbiome in the inocula and after chrysanthemum growth, as well as plant and herbivore parameters. We show that inocula and inoculated soil in which a focal plant had grown harbor remarkably different microbiomes, with the focal plant exerting a strong negative effect on fungi, especially arbuscular mycorrhizal fungi. Soil inoculation consistently induced resistance against the thrips Frankliniella occidentalis, but not against the mite Tetranychus urticae, when compared with sterilized soil. Additionally, plant species shaped distinct microbiomes that had different effects on thrips, chlorogenic acid concentrations in leaves and plant growth. This study provides a proof‐of‐concept that the plant–soil feedback concept can be applied to steer soil microbiomes with the goal of inducing resistance above ground against herbivorous insects.