Significance Although plant growth–promoting bacteria (PGPB) enhance the performance of plants, only a few mechanisms have been identified so far. We show that the sulfur metabolisms in both PGPB Enterobacter sp. SA187 and Arabidopsis plants play a key role in plant salt stress tolerance. Salt stress induces a sulfur starvation response in plants that is attenuated by SA187. Arabidopsis sulfur metabolic mutants are hypersensitive to salt stress but can be rescued by SA187. Most plant sulfur metabolism occurs in chloroplasts and is linked to stress-induced accumulation of reactive oxygen species that is suppressed by SA187. This work reveals that plant salt stress tolerance requires the coordinated regulation of the sulfur metabolic pathways in both beneficial microbe and host plant.