Soil salinization is a major global issue that inhibits plant growth, disrupts rhizosphere microbial ecology, and compromises plant health. Utilizing salt-tolerant, plant-growth-promoting microorganisms offers a promising strategy for mitigating salt stress and improving soil productivity. In this study, a salt-tolerant, phosphate-solubilizing fungal strain was isolated from coastal saline-alkaline soil and designated as Penicillium oxalicum PF1. Its salt tolerance and phosphorus mobilizing capacity were characterized, and pot experiments were conducted to elucidate its effects on plant salt tolerance and the underlying mechanisms. The results showed it could survive up to 17 % (w/v) NaCl in culture medium and solubilized different insoluble phosphorus sources in the order Ca-P > Mg-P > Fe-P, with a maximum solubilization of 980.09 mg/L when Ca-P was supplied. Pot experiments and metagenomic analysis revealed that PF1 significantly promoted alfalfa growth in saline soil, it triggered significant restructuring of the alfalfa rhizosphere microbiome, promoting the functional transformation of rhizosphere microbial communities, thereby alleviating salt stress imposed on alfalfa. In summary, P. oxalicum PF1 exhibits robust salt tolerance and high phosphate-solubilizing activity, restructures the alfalfa rhizosphere microbiome, enhances host stress resistance, mitigates salt-induced physiological damage, and ultimately promotes plant growth in saline soil.