The blue-light receptor cryptochrome 1 (CRY1) primarily mediates blue-light inhibition of hypocotyl elongation in Arabidopsis. However, the underlying mechanisms remain largely elusive. We report here that CRY1 inhibits hypocotyl elongation by repressing brassinosteroid (BR) signaling. A genetic interaction assay reveals the negative regulatory effect of CRY1 on the function of BZR1, a core transcription factor in the BR signaling pathway. We demonstrated that CRY1 interacts with the DNA-binding domain of BZR1 to interfere with the DNA-binding ability of BZR1, and represses its transcriptional activity. Furthermore, we found that CRY1 promotes the phosphorylation of BZR1 and inhibits the nuclear accumulation of BZR1. Interestingly, we discovered that CRY1 interacts with the GSK3-like kinase BIN2 and enhances the interaction of BIN2 and BZR1 in a light-dependent manner. Our findings revealed that CRY1 negatively regulates the function of BZR1 through at least two mechanisms: interfering with the DNA-binding ability of BZR1 and promoting the phosphorylation of BZR1. Therefore, we uncover a novel CRY1-BIN2-BZR1 regulatory module that mediates crosstalk between blue light and BR signaling to coordinate plant growth in Arabidopsis.