Salt stress is a serious environmental challenge that hinders crop growth and yield. Plant growth-promoting rhizobacteria (PGPR) can successfully and environmentally friendly boost plant development in saline soils. In this study, a halotolerant Serratia sp. NTN6 was isolated from the rhizosphere soil of halophyte Puccinellia tenuiflora and its plant growth-promoting properties were determined. NTN6 inoculation significantly promoted seed germination and seedling growth in maize under salt stress. Shoot height, stem thickness, root fresh weight, shoot fresh weight, root dry weight, and shoot dry weight of salt-stressed seedlings increased by 36.3%, 32.5%, 146.4%, 193.6%, 25.0%, and 109.6%, respectively, after inoculation with NTN6. NTN6-mediated maize salt tolerance was revealed via transcriptomic, physiological, and biochemical analyses. Under salt stress, NTN6 regulated the transcript levels of genes related to chlorophyll synthesis, photosynthesis apparatus, and carbon assimilation pathways, and thus increasing chlorophyll content, Fv/Fm, and net photosynthetic rate; NTN6 reduced the content of O2•–, H2O2, and MDA by regulating the transcripts and activities of antioxidant enzymes; NTN6 affected the transcriptional response of genes involved in ABA synthesis and signaling to salt stress and reduced ABA level. Finally, NTN6 boosted photosynthetic capacity in salt-stressed maize by modulating photochemical activity, C4 pathway and Calvin cycle as well as mitigating reactive oxygen species damage to the photosystem reaction center. This study first investigated the mechanism of Serratia sp.-induced salt tolerance in maize and these findings demonstrate the valuable contribution of halotolerant PGPR strain from halophytes in improving salinity tolerance in non-halophytic crops.