Background Plant and soil microbiomes can interfere with pathogen life cycles, but their influence on disease epidemiology remains understudied. Here, we analyzed the relationships between plant and soil microbiomes and long-term epidemiological records of grapevine downy mildew, a major disease caused by the oomycete Plasmopara viticola. Results We found that certain microbial taxa were consistently more abundant in plots with lower susceptibility to the disease and that microbial community composition could predict disease susceptibility. Microbial diversity was not strongly linked to epidemiological records, suggesting that susceptibility is more related to the abundance of specific microbial taxa. These key taxa were identified in the topsoil, where the pathogen’s oospores overwinter, and in the phyllosphere, where zoospores infect leaves. By contrast, the leaf endosphere, where the pathogen’s mycelium develops, contained few taxa of interest. Surprisingly, the soil microbiota was a better predictor of downy mildew symptoms than the leaf microbiota, suggesting a significant role of the soil microbiome in this primarily aerial disease. Conclusion Our study integrates long-term epidemiological data with microbiome profiles of healthy plants to reveal fungi and bacteria relevant for the biocontrol of grapevine downy mildew. The resulting database provides a valuable resource for designing microbial consortia with potential biocontrol activity. The framework can be applied to other crop systems to guide the development of biocontrol strategies and reduce pesticide use in agriculture.Read less <