Priestia species isolated from the cowpea rhizosphere altered the transcriptome of cowpea roots by colonization and enhanced nutrient uptake, antioxidant mechanisms, and photosynthesis, protecting cowpea from drought and nutrient deficiency. Cowpea is a significant grain legume crop primarily grown in sub-Saharan Africa, Asia, and South America. Drought and nutrient deficiency affect the growth and yield of cowpea. To address this challenge, we studied the phyto-beneficial effects of stress-tolerant rhizobacteria on the biomass yield of cowpea under water- and nutrient-deficit conditions. Among the bacteria isolated, two rhizobacillus genotypes, C8 (Priestia filamentosa; basonym: Bacillus filamentosus) and C29 (Priestia aryabhattai; basonym: Bacillus aryabhattai) were evaluated for the improvement of seed germination and growth of cowpea under stress. Our study revealed that C8 protected cowpea from stress by facilitating phosphorus and potassium uptake, protecting it from oxidative damage, reducing transpiration, and enhancing CO₂ assimilation. A 17% increase in root biomass upon C8 inoculation was concomitant with the induction of stress tolerance genes in cowpea roots predominantly involved in growth and metabolic processes, cell wall organization, ion homeostasis, and cellular responses to phosphate starvation. Our results indicate a metabolic alteration in cowpea root triggered by P. filamentosa, leading to efficient nutrient reallocation in the host plant. We propose inoculation with P. filamentosa as an effective strategy for improving the yield of cowpea in low-input agriculture, where chemical fertilization and irrigation are less accessible to resource-poor farmers.