AbstractPlants are colonized by diverse fungal and viral communities that influence their growth and survival as well as ecosystem functioning. Viruses interact with both plants and the fungi they host. Our understanding of plant–fungi–virus interactions is very limited, especially in wild plants. Combining metagenomic and culturomic approaches, we assessed the richness, diversity, and composition of leaf‐associated fungal and viral communities from pools of herbaceous wild plants representative of four sites corresponding to cultivated or natural ecosystems. We identified 161 fungal families and 18 viral families comprising 249 RNA‐dependent RNA polymerase‐based operational taxonomic units (RdRp OTUs) from leaves. Fungal culturomics captured 12.3% of the fungal diversity recovered with metagenomic approaches and, unexpectedly, retrieved viral OTUs that were almost entirely different from those recovered by leaf metagenomics. Ecosystem management had a significant influence on both leaf mycobiome and virome, with a higher fungal community richness in natural ecosystems and a higher viral family richness in cultivated ecosystems, suggesting that leaf‐associated fungal and viral communities are under the influence of different ecological drivers. Both the leaf‐associated fungal and viral community compositions showed a strong site‐specificity. Further research is needed to confirm these trends and unravel the factors structuring plant–fungi–virus interactions in wild plant populations.