Significance The brassinosteroid (BR) receptor BRI1 provides a paradigm for understanding receptor-mediated signaling in plants. Different posttranslational modifications have been implicated in the regulation of BRI1 activity. Here, we show that BR perception promotes BRI1 association with plant U-box E3 ubiquitin ligases PUB12 and PUB13, which in turn directly ubiquitinate BRI1. Importantly, the BRI1 protein abundance and plasma membrane-residence time are increased while the endosomal pool of BRI1 is reduced in the pub12pub13 mutant, indicating that PUB12/PUB13-mediated ubiquitination regulates BRI1 endocytosis and degradation. BRI1 phosphorylates PUB13 on a specific residue to enhance its association with BRI1, suggesting a unique regulatory circuit of phosphorylation-regulated E3 ligase–substrate association. Our study elucidates a mechanism of BRI1 internalization through E3 ubiquitin ligase-mediated ubiquitination.