Soil salinization and phytopathogen infection threaten global crop productivity. Plant growth-promoting rhizobacteria that alleviate abiotic stress while suppressing disease offer a sustainable solution. We aimed to identify a strain with robust salt tolerance, broad-spectrum antagonism, and effective root colonization. A novel halotolerant bacterium isolated from plant rhizosphere at an artificial lakeside was evaluated for plant growth-promoting and biocontrol capacities through phenotypic assays. High-quality whole genome sequencing and bioinformatic analysis were used for functional annotation. The results showed that Strain 105, identified as Bacillus halotolerans, exhibited exceptional tolerance to NaCl concentrations up to 14% (w/v). Under 200 mmol/L NaCl stress, inoculation significantly enhanced wheat seedling growth, increasing root length by 20% and plant height by 18% compared to controls. Strain 105 displayed strong in vitro antagonistic activity against four phytopathogenic fungi that infect crops during the growing period, three postharvest phytopathogenic fungi, and three pathogenic bacteria. Genomic analysis revealed a 4.2-Mb chromosome encoding four key functional modules: (i) osmoprotective systems for glycine betaine and proline metabolism; (ii) an indole-3-pyruvate pathway for indole-3-acetic acid biosynthesis; (iii) multiple secondary metabolite biosynthetic gene clusters (e.g., iturin, fengycin, bacillibactin, and bacilysin); and (iv) a complete set of genes for chemotaxis, biofilm formation, and root adhesion. In conclusion, the multifunctionality of B. halotolerans Strain 105 arises from the synergistic interplay of genetic modules, enabling it to thrive in saline conditions while promoting plant growth and suppressing diverse pathogens. Strain 105 is a promising candidate for developing next-generation microbial inoculants for sustainable agriculture in saline-alkali soils.