Brassinosteroids (BR) have centrally important functions in plant growth by promoting cell proliferation and cell expansion through phosphorylation-mediated regulatory cascades that are initiated by perception of BR by receptor-like kinases of the BRI1 family. These BR-mediated growth responses have been explained by transcriptional controls mediated by phosphorylation of BES1/BZR1 transcription factors. Here we link BRI1-mediated phosphorylation to another growth regulatory network that directly mediates protein stability. BRI1 and its co-receptor BAK1 phosphorylate and inhibit the activities of the growth repressor DA1 by promoting the formation of high molecular weight complexes. Phospho-mimic forms of DA1 are less active while phospho-dead mutants have increased growth-repressive activity, while their regulatory monoubiquitylation is unaffected. BR inhibition of DA1 activity maintains higher levels of DA1 substrates such as UBP15 that sustain the potential for cell proliferation during leaf growth. Reduced BR levels lead to activation of DA1 peptidase activity and a transition from cell proliferation to cell growth and differentiation. This dual monoubiquitylation-phosphorylation regulation supports the key role of BR levels in maintaining the proliferative potential of cells during organ growth.