Phosphorus (P) deficiency and soil-borne fungal diseases are major constraints to peanut (Arachis hypogaea L.) production. Phosphate-solubilizing bacteria (PSB) can improve P availability in the soil, thereby promoting plant growth. However, their potential to improve plant resistance against pathogens under P-limited conditions remains poorly understood. In this study, we first evaluated the ability of two PSB strains, Enterobacter sp. J49 and Serratia sp. S119, to induce systemic resistance (ISR) in peanut plants against the fungal pathogen Sclerotium rolfsii. Results showed that strain S119 reduced disease severity by 40%, whereas strain J49 reduced both incidence (30%) and severity (40%). The protective effect produced by strain J49 was mediated by ISR, as evidenced by the early increase in phenolic compounds accumulation (48 h) and total peroxidase activity (72 h) in inoculated plants. Under P-deficient conditions, the J49 strain was also able to protect peanut plants against S. rolfsii, as demonstrated by a significant reduction in disease severity (55%). These findings highlight the potential of multifunctional bacterium Enterobacter sp. J49 to enhance sustainable peanut production by simultaneously improving P acquisition and strengthening plant defense mechanisms.