Aims Plant Growth-Promoting Rhizobacteria (PGPR) support plant growth by alleviating plant stresses, among which those triggered by saline soils. We isolated Stenotrophomonas sp. SRS1 from salt-resistant Carex distans (distant sedge) roots to understand how this growth promotion was enabled and whether an active contribution of the bacteria and/or plant was required. Methods Various growth assays were used to analyze the effect of bacterial inoculation on Arabidopsis thaliana and Solanum lycopersicum (cherry tomato MicroTom) growth. Furthermore, droplet microfluidics, bacterial genome mining, and bacterial and plant gene expression analysis combined with plant mutant analysis were used for in-depth analysis. Results SRS1 application enhanced plant growth in both saline and nonsaline environments. The fresh weight of SRS1-inoculated plants was higher than that of noninoculated plants, whereas the fresh weight ratio between SRS1-inoculated and noninoculated plants differed whether the plants were grown on agar plates, white sand or in soil. We demonstrated that the strain grew well in high salt-containing media and that, besides plant-growth-promotion-related genes, the bacterium contained various active stress genes. Interestingly, inoculation with the strain increased the induction of plant genes related to abscisic acid and auxin signaling pathways under saline conditions. Conclusions SRS1 inoculation promoted the growth of Arabidopsis and MicroTom tomato under saline and nonsaline conditions, also when the plants were grown in white sand and potting soil. Overall, genetic traits related to stress alleviation, derived from both the bacteria and the plants, play a crucial role in the impact of this novel PGPR strain on plant performance.