MORPHEUS’ MOLECULE1 (MOM1) is anArabidopsisfactor previously shown to mediate transcriptional silencing independent of major DNA methylation changes. Here we find that MOM1 localizes with sites of RNA-directed DNA methylation (RdDM). Tethering MOM1 with an artificial zinc finger to an unmethylatedFWApromoter leads to establishment of DNA methylation andFWAsilencing. This process is blocked by mutations in components of the Pol V arm of the RdDM machinery, as well as by mutation ofMICRORCHIDIA 6 (MORC6). We find that at some endogenous RdDM sites, MOM1 is required to maintain DNA methylation and a closed chromatin state. In addition, efficient silencing of newly introducedFWAtransgenes is impaired in themom1mutant. In addition to RdDM sites, we identify a group of MOM1 peaks at active chromatin near genes that colocalized with MORC6. These findings demonstrate a multifaceted role of MOM1 in genome regulation.