DNA methylation shapes the epigenetic landscape of the genome and plays critical roles in regulating gene expression and ensuring transposon silencing. While DNA methylation patterns are known to differ between tissues, cell-types, and loci, how these differences arise remains poorly understood. In plants, DNA methylation is established via the RNA-directed DNA methylation (RdDM) pathway. In this pathway, RNA POLYMERASE-IV (Pol-IV) plays a critical role in specifying DNA methylation patterns as it initiates the biogenesis of 24-nucleotide small interfering RNAs (24nt-siRNAs) that guide methylation at cognate genomic loci. Affinity purification and characterization of cofactors associated with this specialized RNA polymerase have revealed key insights into how the RdDM pathway is regulated. Focusing on the CLASSY (CLSY) family of putative chromatin remodeling factors, our work has revealed how controlling the composition of the Pol IV complex and regulating its targeting to chromatin in both a locus- and tissue-specific manner enables the generation of diverse patterns of DNA methylation during plant development.