White lupin (Lupinus albus L.) produces cluster roots to acquire more phosphorus under phosphorus deficiency. Bacillus amyloliquefaciens SQR9 contributes to plant growth, but whether and how it promotes cluster root formation in white lupin remain unclear. Here, we investigated the roles of SQR9 in cluster root formation under low phosphorus conditions using a microbial mutant and virus-induced gene silencing (VIGS) in white lupin. SQR9 substantially enhanced cluster root formation under low phosphorus conditions. The ysnE gene encodes an auxin biosynthesis enzyme in SQR9 and was associated with cluster root formation, as ysnE-defective SQR9 did not trigger cluster root formation. SQR9 inoculation induced the expression of PIN-formed2 (LaPIN2, encoding an auxin transporter) and YUCCA4 (LaYUC4, encoding an auxin biosynthesis enzyme) in white lupin roots. VIGS-mediated knockdown of LaPIN2 and LaYUC4 prevented wild-type SQR9-induced cluster root formation in white lupin. Finally, white lupin LaYUC4-derived auxin and SQR9-derived auxin pools were both transported by LaPIN2, promoting cluster root formation under low phosphorus conditions. Taken together, we propose that B. amyloliquefaciens promotes cluster root formation in white lupin under low phosphorus conditions by stimulating auxin biosynthesis and transport. Our results provide insights into the interplay between bacteria and root auxin in crop phosphorus use efficiency.