As climate change intensifies, forest ecosystems face increasing destabilization and biodiversity loss. While the role of tree species richness in maintaining ecosystem stability is well-established, the influence of shrub diversity—particularly under varying tree species richness—remains insufficiently understood. Here, we investigate the intricate interplay between shrub species richness, soil microbial communities, and environmental factors in driving ecosystem stability, defined as the temporal stability of tree community productivity. Using a large-scale, controlled experimental platform (BEF-China), we examined these dynamics across a gradient of tree species richness: monocultures, two-species mixtures, and four-species mixtures. Our findings reveal that shrub species richness exerts context-dependent effects on ecosystem stability, strengthening stability at higher levels of tree species richness. These effects are mediated primarily by shifts in microbial diversity and community-aggregated genomic traits. In monocultures, stability was predominantly governed by abiotic factors such as soil pH and slope, with minimal contributions from shrub species richness. In contrast, in two-species mixtures, increased shrub species richness significantly enhanced stability by promoting bacterial diversity and restructuring fungal communities. In four-species mixtures, bacterial and fungal genomic traits differentially modulated stability, highlighting the pivotal yet distinct roles of microbial communities in mediating biodiversity-stability relationships. Additionally, we identified key microbial taxa whose contributions to stability varied with tree species richness, further emphasizing the complexity of these interactions. Together, our results underscore the dynamic and context-specific roles of shrub diversity and microbial mediators in shaping ecosystem stability, providing novel insights into the mechanisms underpinning forest resilience in an era of rapid environmental change.