High-temperature stress, also referred to as heat stress, often has detrimental effects on plant growth and development. Phytochromes have been implicated in the regulation of plant heat-stress responses, but the role of blue-light receptors, such as cryptochromes, in plant blue-light-dependent heat-stress responses remains unclear. We found that cryptochrome 1 (CRY1) negatively regulates heat-stress tolerance (thermotolerance) in Arabidopsis. Heat stress represses CRY1 phosphorylation. Unphosphorylated CRY1 exhibits decreased activity in suppressing the interaction of CONSTITUTIVE PHOTOMORPHOGENIC 1 (COP1) with ELONGATED HYPOCOTYL 5 (HY5), leading to excessive degradation of HY5 under heat stress in blue light. This reduction in HY5 protein levels subsequently relieves its repression of the transcription of HY5 target genes, especially the heat-shock transcription factors. Our study thus reveals a novel mechanism by which CRY1-mediated blue-light signaling suppresses plant thermotolerance and highlights the dual function of the CRY1-COP1-HY5 module in both light- and heat-stress signaling, providing insights into how plants integrate heat stress and light signals to optimize their survival under heat stress.