Eukaryotic cytosine methylation represses transposable elements, but also occurs in bodies of active genes. The extent to which these processes are conserved is unclear, and little is known about methylation outside of mammals, Arabidopsis thaliana, and Neurospora crassa. Utilizing deep bisulfite sequencing, we have quantified DNA methylation in five plant, seven animal, and five fungal genomes. We find that gene body methylation is conserved between plants and animals, whereas selective methylation of transposons has evolved independently in the vertebrate lineage. We show that methylation of plant transposons in the CHG context extends to green algae, and present evidence for RNA-directed DNA methylation of fungal genes. We also show that antagonism between DNA methylation and histone H2A.Z is conserved between plants and animals. Our data demonstrate that extant DNA methylation systems are mosaics of conserved and derived features, and indicate that gene body methylation is an ancient property of eukaryotic genomes. Keywords: Epigenetics Overall design: Examination of DNA methylation and transcription in plant, animal, and fungal genomes, and examination of how H2A.Z deposition relates to both methylation and transcription in puffer fish. Descriptions of the Samples' raw and processed data (provided as supplementary files) can be found in GSE19824_README.txt at the foot of this record.