Background: Since the 1980s, soils in a 22-km 2 area near Lake Neuchâtel in Switzerland have been recognized for their innate ability to suppress the black root rot plant disease caused by the fungal pathogen Thielaviopsis basicola . However, the efficacy of natural disease suppressive soils against insect pests has not been studied. Results: We demonstrate that natural soil suppressiveness also protects plants from the leaf-feeding pest insect Oulema melanopus . Plants grown in the most suppressive soil have a reduced stress response to Oulema feeding, reflected by dampened levels of herbivore defense-related phytohormones and benzoxazinoids. Enhanced salicylate levels in insect-free plants indicate defense-priming operating in this soil. The rhizosphere microbiome of suppressive soils contained a higher proportion of plant-beneficial bacteria, coinciding with their microbiome networks being highly tolerant to the destabilizing impact of insect exposure observed in the rhizosphere of plants grown in the conducive soils. We suggest that presence of plant-beneficial bacteria in the suppressive soils along with priming, conferred plant resistance to the insect pest, manifesting also in the onset of insect microbiome dysbiosis by the displacement of the insect endosymbionts. Conclusions Our results show that an intricate soil–plant-insect feedback, relying on a stress tolerant microbiome network with the presence of plant-beneficial bacteria and plant priming, extends natural soil suppressiveness from soilborne diseases to insect pests.