DNA methylation is a type of stable epigenetic modifications that plays crucial roles in regulating gene expression, silencing transposons and maintaining genome stability. In plants, the de novo DNA methylation is established via a pathway termed as RNA-directed DNA methylation (RdDM). The plant-specific DNA-dependent RNA polymerase IV (Pol IV) as the core protein in RdDM pathway produces non-coding RNAs that direct the establishment of DNA methylation, regulates gene expression and controls plant development. Pol IV function is regulated by several proteins including SHH1, which recognizes H3K9 methylation and guides Pol IV to genome specific sites, the chromatin remodeling factor CLSY family that is involved in assisting Pol IV chromatin association and RDR2 that converts Pol IV produced single-stranded RNA into double-stranded RNA. In this review, we summarize the latest progress on Pol IV and its co-regulators, and focus on their functions in shaping epigenome and development in plants, which might provide implications for studying of DNA methylation and crop breeding.