Advances in DNA sequencing technologies have led to the first single-base resolution maps of cytosine DNA methylation. These maps are revealing a diverse set of mechanisms that genomes utilize to control genome stability, transposon silencing, and gene expression. Our previous studies in natural and experimental Arabidopsis thaliana populations have uncovered errors in maintenance of DNA methylation that lead to the existence of spontaneous epigenetic alleles. The rates of formation of single methylation polymorphisms are about five orders of magnitude greater than the spontaneous mutation rate, whereas the formation of differentially methylated regions that affect gene expression occurs at a frequency that is similar to the spontaneous DNA mutation rate. To better understand the mechanisms governing maintenance of DNA methylation over longer evolutionary timescales, we sequenced and used publicly available DNA methylomes of 34 flowering plant species and the basal flowering plant Amborella trichopoda. Additionally, we have developed a novel high-throughput analysis method for profiling DNA methylation levels for any species regardless of the availability of a reference genome. We are unraveling the mechanistic underpinnings that evolved to establish and maintain DNA methylation by using this base modification as a molecular phenotype in combination with phylogenetic and molecular analysis of enzymes involved in DNA methylation.