Aims <p>NaHCO₃ causes stress in plants, significantly affecting agricultural production. While microorganisms have been shown to mitigate such stress, the underlying microbiome-mediated mechanisms remain unclear.</p> Methods <p>In this study, a NaHCO₃-tolerant strain NYJ was inoculated into cucumber-planted soil contaminated with NaHCO₃. Its effects on the rhizospheric microbiome, antioxidant enzymes and soil enzymes were analyzed.</p> Results <p>Under NaHCO₃ stress, 16 genera were depleted and one genus was enriched, all of which were enriched after NYJ application. Consistently, NYJ application changed microbial interaction networks and shifted the symbiont-related, osmotic stress-responsive and sodium ion-responsive functions of soil microbial communities under NaHCO₃ stress. As a result, NYJ application under NaHCO₃ stress significantly improved plant growth, affected Na⁺ concentrations in cucumber and decreased hydrogen peroxide levels in seedlings. Additionally, the NYJ application enhanced the activities of seven antioxidant enzymes in leaves, induced catalase in soil and enriched genes responding to reactive oxygen species in GO:0052550 and GO:0052567 of soil microbial communities in a NaHCO₃ environment, thereby reducing NaHCO₃-induced oxidative stress. In the meantime, NYJ application significantly induced soil enzymes including ureases, phosphatases and sucrases and increased the abundances of chitinase genes in K01183 of microbial communities in NaHCO₃-contaminated soil, facilitating the promotion of plant growth.</p> Conclusion <p>These findings suggest that NYJ application modifies the soil microbiome and enhances its resilience against NaHCO₃ stress, offering a promising strategy for improving crop tolerance in alkaline soils. This study provides novel insights into the microbiome-mediated mitigation of NaHCO₃ stress through the application of NYJ.</p>