Arsenite (AsIII)-oxidizing bacteria show great potential for mitigating arsenic (As) accumulation in rice plants; however, their molecular mechanisms remain unclear. In this study, our soil pot experiment demonstrated that inoculation with the AsIII-oxidizing bacterium SMS11 decreased porewater As by 94.8% (from 448 to 23.4 μg·kg-1), further reducing shoot As by 40.6% (from 6.02 to 3.58 mg·kg-1) and increasing shoot biomass by 78.3% (from 2.34 to 4.17 g). In the hydroponic experiment, ionomics revealed that SMS11 inoculation mitigated AsIII-induced changes in the ion content (e.g., P, K, Mg, and Ca) in both rice shoots and roots. Transcriptomics showed an 85% decrease in differentially expressed genes (8332 vs 1247) in shoots. Additionally, key As accumulation genes (e.g., OsLsi1, OsPT4, OsPT8, and OsHAC4) were downregulated by 26.9-84.0%, and disrupted biological processes (e.g., oxidative stress response, ion binding, and photosynthesis) were restored. Altogether, SMS11 inoculation boosts rice resilience by reshaping ionomic and transcriptomic homeostasis under AsIII stress.