Background and aims <p>The management of soil-borne plant pathogens is a significant challenge in modern agriculture, particularly given the limitations of chemical control strategies. In this context, the management of the soil microbiome can be an important tool towards the biological control of soil-borne plant pathogens. In this study, we isolated bacterial strains from soil microbiomes with potential biocontrol activity against <i>Armillaria mellea</i>, a destructive fungal pathogen responsible for root rot in multiple crops.</p> Methods <p>Using a mass selection approach, we identified 155 bacterial isolates with antifungal activity, which we further screened to select four <i>Pseudomonas</i> spp. isolates that exhibited strong in vitro inhibitory effects on <i>A. mellea</i>. Whole-genome sequencing of these isolates revealed biosynthetic gene clusters encoding antifungal metabolites and siderophores that are potentially involved in pathogen suppression and plant growth promotion. We further assessed their effect on plant microbiomes and growth performance in a microcosm experiment with olive plants (<i>Olea europaea</i>).</p> Results <p>Our results show that inoculation with live bacterial isolates, compared to inactivated isolates, increased plant biomass while exerting limited effects on native root and rhizosphere microbiomes. Additionally, we observed indirect effects on plant biomass through plant-associated microbial communities, suggesting a complex interplay between the host and bacterial isolates in the rhizosphere, with an eventual impact on plant health.</p> Conclusions <p>Soil-derived <i>Pseudomonas</i> spp. can be effective biocontrol agents against <i>A. mellea</i>, and their ability to enhance plant growth while maintaining microbiome stability makes them promising candidates for field application, promoting microbiome-based solutions in modern agriculture.</p>