In our previous study we showed that volatile organic compounds (VOCs) from Alcaligenes faecalis JBCS1294 (JBCS1294) induced tolerance to salt stress in Arabidopsis thaliana by influencing the auxin and gibberellin pathways and upregulating the expression of key ion transporters. The aim of this study was to evaluate the contribution of each VOC and blends of the VOCs on the induction of salt tolerance and signaling pathways. The key VOCs emitted from JBCS1294 were dissolved in lanolin and applied to one side of bipartite I-plates that contained Arabidopsis seeds on Murashige and Skoog (MS) media supplemented with NaCl on the other side. Changes in plant growth were investigated using Arabidopsis mutant lines and hormone inhibitors, and gene expression was assessed by real-time PCR (qPCR). Among the VOCs, butyric acid conferred salt tolerance over a concentration range of 5.6μM (10ng)–56mM (100μg), whereas propionic and benzoic acid were effective at micromolar doses. Intriguingly, the optimized cocktail of the three VOCs increased fresh weight of Arabidopsis under salt stress compared to that achieved with each single compound. However, Arabidopsis growth was not promoted by the VOCs without salt stress. Exogenous indole-3-acetic acid (IAA) application arrested salt tolerance or growth promotion of Arabidopsis induced by volatiles from propionic acid, but not from butyric acid and an optimized volatile mixture of butyric acid, propionic acid, and benzoic acid (1PBB). High and intense auxin-responsive DR5:GUS activity was observed in the roots of Arabidopsis grown on media without salt via 1PBB, butyric acid, and benzoic acid. Growth promotion by the cocktail was inhibited in the eir1 mutant and in Col-0 plants treated with inhibitors of auxin and gibberellin. The present study clearly demonstrated the effects of individual VOCs and blends of VOCs from a rhizobacterial strain on the induction of salt stress. The results with the blend of VOCs, which mimics bacterial emissions in nature, may lead to a deeper understanding of the interaction between rhizobacteria and plants.