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Significance DNA methylation and histone modifications are two key epigenetic mechanisms in regulating gene expression, heterochromatin assembly, and genome stability. In mammals, maintenance of DNA methylation is mainly mediated by DNA methyltransferase 1 (DNMT1) in a replication-dependent manner. The spatiotemporal regulation of DNMT1 is essential for faithful propagation of DNA methylation patterns between cell generations. Here, we report the direct readout of the heterochromatic mark H3K9me3 by the RFTS domain of DNMT1, which serves to enhance the enzymatic stimulation of DNMT1 by previously characterized H3 ubiquitylation and mediates the cellular colocalization of DNMT1 and H3K9me3. This study uncovers a direct link between the repressive histone modification and DNMT1-mediated DNA methylation.