Halotolerant plant growth-promoting bacteria (HT-PGPB) have attracted considerable attention for their significant potential in mitigating salt stress in crops. However, the current exploration and development of HT-PGPB remain insufficient to meet the increasing demands of agriculture. In this study, an HT-PGPB isolated from coastal saline-alkali soil in the Yellow River Delta was identified as Glutamicibacter endophyticus J2-5-19. The strain was capable of growing in media with up to 13% NaCl and producing proteases, siderophores, and the plant hormone IAA. Under 4‰ salt stress, inoculation with strain J2-5-19 significantly increased the wheat seed germination rate from 37.5% to 95%, enhanced the dry weight of maize seedlings by 41.92%, and notably improved the development of maize root systems. Moreover, this work presented the first whole-genome of Glutamicibacter endophyticus, revealing that G. endophyticus J2-5-19 resisted salt stress by expelling sodium ions and taking up potassium ions through Na⁺/H⁺ antiporters and potassium uptake proteins, while also accumulating compatible solutes such as betaine, proline, and trehalose. Additionally, the genome contained multiple key plant growth-promoting genes, including those involved in IAA biosynthesis, siderophore production, and GABA synthesis. The findings provide a theoretical foundation and microbial resources for the development of specialized microbial inoculants for saline-alkali soils.