In eukaryotes, DNA repair pathways help to maintain genome integrity and epigenomic patterns. However, the factors at the nexus of DNA repair and chromatin modification/remodeling remain poorly characterized. Here, we uncover a previously unrecognized interplay between the DNA repair factor DNA DAMAGE-BINDING PROTEIN 2 (DDB2) and the DNA methylation machinery in Arabidopsis thaliana. Loss-of-function mutation in DDB2 leads to genome-wide DNA methylation alterations. Genetic and biochemical evidence indicate that at many repeat loci, DDB2 influences de novo DNA methylation by interacting with ARGONAUTE 4 (AGO4) and by controlling the local abundance of 24-nt short interfering RNAs (siRNAs). We also show that DDB2 regulates active DNA demethylation mediated by REPRESSOR OF SILENCING 1 (ROS1) and DEMETER LIKE-3 (DML3). Together, these findings reveal a role for the DNA repair factor DDB2 in shaping the A. thaliana DNA methylation landscape in the absence of applied genotoxic stress.