Soil salinization is a critical constraint on global rice production, posing a serious threat to food security and underscoring the urgent need for sustainable strategies to fortify plant stress resilience. In this context, this study demonstrates that SB24, a halotolerant PGPR isolated from saline rice fields, markedly improved the salinity tolerance of rice genotype Pusa 44 through coordinated physiological, biochemical, and molecular responses. This strain, identified by 16S rDNA sequencing, exhibited high salt tolerance (up to 16% NaCl) and possessed multiple plant growth-promoting traits. Under 125 mM NaCl stress, SB24 inoculation enhanced germination and growth, with significant increases in shoot and root biomass compared to uninoculated controls. SB24-treated plants showed elevated photosynthetic pigments (Chl a, Chl b, carotenoids), soluble sugars, and soluble proteins, alongside enhanced antioxidant enzyme activities (SOD, CAT, APX, PPO) significantly. These changes were accompanied by reductions in oxidative stress markers, including electrolyte leakage, H₂O₂ accumulation, lipid peroxidation, and lipoxygenase activity. SB24 also promoted osmolyte accumulation (proline, glycine betaine and maintained ion homeostasis by reducing Na⁺ uptake while increasing K⁺ and Ca2⁺ retention. At the transcriptional level, SB24 upregulated the expression of key salt-responsive genes, including OsSOS1 (salt overly sensitive 1) 1.35-fold, OsNHX1 (vacuolar Na⁺/H⁺ antiporter 1) 1.5-fold, OsHKT1;5 (high-affinity K⁺ transporter 1;5) 1.23-fold, OsFeSOD (iron superoxide dismutase) 1.22-fold, and OsAPX (ascorbate peroxidase) 1.18-fold, validating the observed physiological, and biochemical responses to improved salt stress tolerance. Taken together, these findings establish SB24 as a potent bioinoculant with strong potential for mitigating salinity stress through integrated, multi-level mechanisms.