Background and aims The rhizosphere microbiome has been shown to contribute to nutrient acquisition, protection against biotic and abiotic stresses and, ultimately, to changes in the development and physiology of plants. Here, using a controlled natural selection approach, we followed the microbial dynamics in the soil of Arabidopsis thaliana plants infected with the foliar pathogen Pseudomonas syringae DC3000 (Pst). Methods Plants were iteratively cultivated on a pasteurised soil inoculated with the soil microbial community of the previous iteration isolated from the rhizosphere of plants infected with Pst (pst-line) or not (mock-line). Modification of soil microbial communities was assessed through an amplicon-based metagenomic analysis targeting bacterial and fungal diversity. Plant fitness and transcript abundance of stress hormone related genes were also analysed. Results At the tenth and eleventh iterations respectively, we observed a reduction in disease severity of 81% and 85% in pst-lines as compared to mock-lines. These changes were associated with (i) an early induction of defence mechanisms mediated by salicylic acid, in pst-line as compared to mock-line, shown by the decrease in transcript abundance of salicylic acid related genes, whereas jasmonic acid, ethylene or abscisic acid related genes remained unchanged and (ii) a shift in soil bacterial, and not in fungal, composition. Conclusions Our study suggests that these changes in soil bacterial composition are mediated by plant-soil feedback in response to Pst and resulted in an activation of SA-related immune response in the plant. This supports the concept of applying plant-soil feedbacks to enhance soil suppressiveness against foliar pathogens.