The study investigates the role of the Arabidopsis Nucleosome Remodeler DDM1 in DNA methylation and its interaction with other methylation pathways. DDM1 is shown to facilitate DNA methylation in all sequence contexts, particularly in heterochromatic sequences, and this function is independent of small-RNA-directed DNA methylation (RdDM). The methyltransferase CMT2 is identified as the enzyme responsible for DDM1-mediated, RdDM-independent CHH methylation. DDM1 and RdDM synergistically mediate nearly all transposon methylation and collaborate to repress transposition and regulate gene expression. The results indicate that DDM1 allows DNA methyltransferases access to H1-containing heterochromatin, enabling stable silencing of transposable elements. The study also reveals that DDM1 is important for DNA methylation in genes, with its requirement positively correlated with heterochromatin levels. Overall, the findings highlight the importance of DDM1 in maintaining genomic stability and gene regulation through its role in DNA methylation.The study investigates the role of the Arabidopsis Nucleosome Remodeler DDM1 in DNA methylation and its interaction with other methylation pathways. DDM1 is shown to facilitate DNA methylation in all sequence contexts, particularly in heterochromatic sequences, and this function is independent of small-RNA-directed DNA methylation (RdDM). The methyltransferase CMT2 is identified as the enzyme responsible for DDM1-mediated, RdDM-independent CHH methylation. DDM1 and RdDM synergistically mediate nearly all transposon methylation and collaborate to repress transposition and regulate gene expression. The results indicate that DDM1 allows DNA methyltransferases access to H1-containing heterochromatin, enabling stable silencing of transposable elements. The study also reveals that DDM1 is important for DNA methylation in genes, with its requirement positively correlated with heterochromatin levels. Overall, the findings highlight the importance of DDM1 in maintaining genomic stability and gene regulation through its role in DNA methylation.