Soil salinity is a major environmental stressor impacting global food production. Staple crops like wheat experience significant yield losses in saline environments. Bioprospecting for beneficial microbes associated with stress-resistant plants offers a promising strategy for sustainable agriculture. We isolated two novel endophytic bacteria, Bacillus cereus (ADJ1) and Priestia aryabhattai (ADJ6), from Agave desmettiana Jacobi. Both strains displayed potent plant growth-promoting (PGP) traits, such as producing high amounts of indole-3-acetic acid (9.46, 10.00 µgml−1), ammonia (64.67, 108.97 µmol ml−1), zinc solubilization (Index of 3.33, 4.22, respectively), ACC deaminase production and biofilm formation. ADJ6 additionally showed inorganic phosphate solubilization (PSI of 2.77), atmospheric nitrogen fixation, and hydrogen cyanide production. Wheat seeds primed with these endophytes exhibited enhanced germination, improved growth profiles, and significantly increased yields in field trials. Notably, both ADJ1 and ADJ6 tolerated high salinity (up to 1.03 M) and significantly improved wheat germination and seedling growth under saline stress, acting both independently and synergistically. This study reveals promising stress-tolerance traits within endophytic bacteria from A. desmettiana. Exploiting such under-explored plant microbiomes offers a sustainable approach to developing salt-tolerant crops, mitigating the impact of climate change-induced salinization on global food security.