DUF506 proteins are omnipresent in higher plants. Phosphorus (P) stress-inducible AtRXR1/REPRESSOR OF EXCESSIVE ROOT HAIR ELONGATION 1 gene, as the first functionally characterized DUF506 gene, is proved to inhibit root hair elongation through interaction of RXR2/RabD2c GTPase. However, the knowledge of other P-responsive DUF506 genes is still limited. Here, we identify four additional P-inducible DUF506 genes and select two of candidates for functional investigation. Expression analysis results reveal that both of candidates are induced by auxin. At3g07350, the duplicated pair of RXR1, expresses ubiquitously in seedlings under P-stress, whereas At1g62420 is mainly induced in roots. Overexpression and knockout mutants of At1g62420, which is called RXR3, exhibit shorter or longer root hair length, respectively. Cellular imaging results demonstrate RXR3 localizes in root epidermal cells. ChIP, synthetic peptide treatment and qRT-PCR assay results indicate RXR3 is transcriptionally activated by RSL4 or RALF1. BiFC and CaM-binding assay suggest that RXR3 interacts with various CaMs in presence of Ca2+. Moreover, the frequencies of [Ca2+]cyt in rxr3 mutants are approximately 20% higher compared to that of wild type. Taken together, our results illustrate a divergent mechanism by which RSL4-directed RXR3 interacts with calmodulin and functions in parallel of RXR1, to prevent root hair excessive growth.