Aims <p>Soil-borne pathogens can severely compromise legume cultivation and, consequently, plant-based protein production by triggering root rot, particularly in pea (<i>Pisum sativum</i> L.). Although some pea genotypes exhibit enhanced performance compared to others under root rot stress, breeding efforts have so far achieved only limited resistance. Microbiome-mediated breeding might show more success in alleviating root rot. We hypothesized that some root‑associated microbes serve as resistance markers across diverse soils. We therefore determined whether certain fungi or mycobiome attributes consistently associated with a genotype's resistance across a diverse range of soils.</p> Methods <p>Root-associated fungal communities of eight pea genotypes differing in root rot resistance were characterized by ITS amplicon sequencing in four soils with contrasting infestation levels under controlled conditions. We employed alpha and beta diversity, as well as differential abundance analyses, to detect genotype- and soil-specific patterns and associations with resistance traits.</p> Results <p>Both genotype and soil identity influenced alpha diversity. Evenness was reduced in infested soils, as OTU richness increased. Fungal community composition covaried with infestation level, genotype and previously defined resistance levels of the genotypes. A single OTU (OTU3), showing 100% sequence similarity to a previously identified heritable, resistance-associated hub taxon (<i>Dactylonectria</i>), was consistently enriched in resistant genotypes across soils and was positively correlated with seed emergence.</p> Conclusions <p>Our results reveal OTU3 as a common microbial resistance marker, highlighting the potential of microbiome-mediated root rot resistance breeding in legumes. The uncovered phenomenon may represent a promising avenue to promote sustainable legume cultivation.</p>