DNA methylation is a chemical modification of DNA that can be faithfully inherited across generations in flowering plant genomes. Failure to properly maintain DNA methylation can lead to epigenetic variation and transposon reactivation. Plant genomes are dynamic, spanning large ranges in size and there is an interplay between the genome and epigenome in shaping one another. To understand the variation in genomic patterning of DNA methylation between species, we compared methylomes of numerous diverse angiosperm species. By examining these variations in a phylogenetic context it becomes clear that there is extensive variation in mechanisms that govern gene body DNA methylation, euchromatic silencing of transposons and repeats, as well as silencing of heterochromatic transposons. Extensive variation is observed at all cytosine sequence contexts (CG, CHG and CHH, where H = A, C, T), with the Brassicaceae showing reduced CHG methylation levels and also reduced or loss of CG gene-body methylation. The Poaceae are characterized by a lack or reduction of heterochromatic CHH methylation and enrichment of CHH methylation in genic regions. Reduced CHH methylation levels are found in clonally propagated species, suggesting that these methods of propagation may alter the epigenomic landscape over time, in the absence of sexual reproduction. These results show that DNA methylation targeting pathways have diverged functionally and that extant DNA methylation patterns are likely a reflection of the evolutionary and life histories of plant species. Overall design: Bisulfite-seq of leaf tissue from plants representing diverse angiosperms. RNA-seq and small RNA-seq was performed on leaf tissue of a subset of the species.