The evolution of gene body methylation (gbM) and the underlying mechanism is poorly understood. By pairing the largest collection of CHROMOMETHYLTRANSFERASE (CMT) sequences (773) and methylomes (72) across land plants and green algae we provide novel insights into the evolution of gbM and its underlying mechanism. The angiosperm- and eudicot-specific whole genome duplication events gave rise to what are now referred to as CMT1, 2 and 3 lineages. CMTe, which includes the eudicot-specific CMT1 and 3, and orthologous angiosperm clades, is essential for the perpetuation of gbM in angiosperms, implying that gbM evolved at least 236 MYA. Independent losses of CMT1, 2 and 3 in eudicots, and CMT2 and CMTmonocot+magnoliid in monocots suggests overlapping or fluid functional evolution. The resulting gene family phylogeny of CMT transcripts from the most diverse sampling of plants to date redefines our understanding of CMT evolution and its evolutionary consequences on DNA methylation. Overall design: MethylC-Seq collected from leaves of a diverse collection of land plants. The assembled transcriptomes used in this study were not publicly available at the time of submission since they are part of the on-going 1KP initiative (www.onekp.com). They will be made available upon release of the 1KP capstone paper.