Lateral root (LR) formation is coordinated by both endogenous and external factors. As biotic factors, Plant growth-promoting rhizobacteria (PGPRs) can affect LR formation, while the regulation mechanism is unclear. In this study, by applying various marker lines, we found that volatile compounds (VCs) from PGPR strain Bacillus amyloliquefaciens SQR9 induced a high frequency of oscillation and prebranch site formation, and further accelerated the development and emergence of the lateral root primordia (LRP), thus promoting LR development in model plant Arabidopsis. We demonstrated a critical role of auxin on SQR9 VCs-induced lateral root formation via respective mutants and pharmacological experiments. Our results showed that the YUC9 (YUCs)-mediated auxin biosynthesis, polar auxin transport, and auxin signaling pathway are involved in SQR9 VCs-induced LRs formation. We further showed that acetoin, a major component of SQR9 VCs, is less active in promoting root development compared to SQR9 cells, suggesting uncharacterized VCs might contribute to SQR9 effect in mediating LR formation. In summary, our study revealed a novel mechanism of PGPR-produced VCs in regulating LR branching in a non-contact manner, and further efforts will explore useful VCs to promote plant root development.