Cytosine DNA methylation (5mC) is a widespread base modification in eukaryotic genomes with critical roles in transcriptional regulation. In recent years, our understanding of 5mC has changed due to advances in 5mC detection techniques that allow mapping of this mark on the whole genome scale. Profiling DNA methylomes from organisms across the eukaryotic tree of life has reshaped our views on the evolution of 5mC. In this review we explore the macro-evolution of 5mC in major eukaryotic groups, and then focus on recent advances made in animals. Genomic 5mC patterns as well as the mechanisms of 5mC deposition tend to be evolutionary labile across large phylogenetic distances, however, some common patterns are starting to emerge. Within the animal kingdom, 5mC diversity has proven to be much greater than anticipated. For example, a previously held common view that genome hypermethylation is a trait exclusive to vertebrates has recently been challenged. Also, data from genome-wide studies are starting to yield insights into the potential roles of 5mC in invertebrate cis regulation. Here we provide an evolutionary perspective of both the well-known and enigmatic roles of 5mC across the eukaryotic tree of life.