DNA methylation and histone modification are important epigenetic marks that coregulate gene expression and genome stability. To identify factors involved in chromatin silencing, we carried out a forward genetic screen for mutants that release the silenced Pro-35S:LUCIFERASE (35SP-LUC) in Arabidopsis (Arabidopsis thaliana). We identified an epigenetic regulator, METHIONINE SYNTHASE1 (ATMS1), which catalyzes the synthesis of methionine (Met) in the one-carbon metabolism pathway. The ATMS1 mutation releases the silenced 35SP-LUC and the majority of endogenous genes and transposons. The effect of ATMS1 on chromatin silencing is related to decreased levels of DNA methylation (CG, CHG, and CHH) and histone-3 lysine-9 dimethylation. The ATMS1 mutation caused a significant decrease in the ratio of S-adenosylmethionine to S-adenosylhomocysteine. Exogenous application of Met rescued the phenotype of atms1-1. ATMS1 plays a predominant role in DNA and histone methylations among the three Met synthetase homologs. These results suggest that ATMS1 is required for DNA and histone methylations through its function in the one-carbon metabolism pathway, indicating the complex interplay between metabolism and epigenetic regulation.