DNA methylation is an important epigenetic gene regulatory mechanism conserved in eukaryotes. Emerging evidence shows DNA methylation alterations in response to environmental cues. However, the mechanism of how cells sense these signals and reprogramme the methylation landscape is poorly understood. Here, we uncovered a connection between ultraviolet B (UVB) signalling and DNA methylation involving UVB photoreceptor (UV RESISTANCE LOCUS 8 (UVR8)) and a de novo DNA methyltransferase (DOMAINS REARRANGED METHYLTRANSFERASE 2 (DRM2)) in Arabidopsis. We demonstrated that UVB acts through UVR8 to inhibit DRM2-mediated DNA methylation and transcriptional de-repression. Interestingly, DNA transposons with high DNA methylation are more sensitive to UVB irradiation. Mechanistically, UVR8 interacts with and negatively regulates DRM2 by preventing its chromatin association and inhibiting the methyltransferase activity. Collectively, this study identifies UVB as a potent inhibitor of DNA methylation and provides mechanistic insights into how signalling transduction cascades intertwine with chromatin to guide genome functions.