The study reveals that the Arabidopsis nucleosome remodeler DDM1 plays a critical role in DNA methylation, particularly in heterochromatic regions. DDM1 facilitates DNA methylation in all sequence contexts, including CG, CHG, and CHH, independently of the RNA-directed DNA methylation (RdDM) pathway. This process is mediated by the chromomethylase CMT2, which is responsible for CHH methylation. DDM1 and RdDM work together to mediate nearly all transposon methylation and to repress transposition and regulate gene expression. DDM1 is essential for DNA methylation in both genes and transposable elements (TEs), with the strength of the DDM1 requirement positively correlated with heterochromatin. Heterochromatin inhibits RdDM, and DDM1 allows DNA methyltransferases access to H1-containing heterochromatin, enabling stable silencing of transposable elements in cooperation with the RdDM pathway. The results indicate that DDM1 is specialized for remodeling heterochromatic, H1-bound nucleosomes to allow DNA methyltransferases and other proteins access to the DNA. The study also shows that DDM1 and RdDM mediate methylation of distinct TE sizes and domains, with DDM1 preferentially mediating methylation within the bodies of long TEs. The findings highlight the importance of chromatin structure in determining the extent to which DDM1 is required for DNA methylation. The study further demonstrates that the loss of DDM1 leads to extensive genic CHG hypermethylation, and that the presence of H1 affects the methylation of genes and TEs. Overall, the study provides a comprehensive understanding of the roles of DDM1 and RdDM in DNA methylation and gene regulation in Arabidopsis.The study reveals that the Arabidopsis nucleosome remodeler DDM1 plays a critical role in DNA methylation, particularly in heterochromatic regions. DDM1 facilitates DNA methylation in all sequence contexts, including CG, CHG, and CHH, independently of the RNA-directed DNA methylation (RdDM) pathway. This process is mediated by the chromomethylase CMT2, which is responsible for CHH methylation. DDM1 and RdDM work together to mediate nearly all transposon methylation and to repress transposition and regulate gene expression. DDM1 is essential for DNA methylation in both genes and transposable elements (TEs), with the strength of the DDM1 requirement positively correlated with heterochromatin. Heterochromatin inhibits RdDM, and DDM1 allows DNA methyltransferases access to H1-containing heterochromatin, enabling stable silencing of transposable elements in cooperation with the RdDM pathway. The results indicate that DDM1 is specialized for remodeling heterochromatic, H1-bound nucleosomes to allow DNA methyltransferases and other proteins access to the DNA. The study also shows that DDM1 and RdDM mediate methylation of distinct TE sizes and domains, with DDM1 preferentially mediating methylation within the bodies of long TEs. The findings highlight the importance of chromatin structure in determining the extent to which DDM1 is required for DNA methylation. The study further demonstrates that the loss of DDM1 leads to extensive genic CHG hypermethylation, and that the presence of H1 affects the methylation of genes and TEs. Overall, the study provides a comprehensive understanding of the roles of DDM1 and RdDM in DNA methylation and gene regulation in Arabidopsis.