DNA methylation is a key epigenetic modification required for vertebrate development, deployed and erased in promoters and enhancer regulatory elements in a dynamic manner. Nevertheless, many of these patterns and dynamics are not observed in the sparsely methylated genomes of the few invertebrates analysed to date, where mostly gene bodies of constitutively expressed genes are methylated. To address if this stark contrast between vertebrate and invertebrate epigenomes is an ancestral feature, we have generated developmental series of whole-genome base resolution maps of cytosine methylation and hydroxymethylation for 3 representatives of the earliest branching positions of animal evolution: sponges, ctenophores and cnidarians. Despite the three species have a conserved toolkit of DNA methyltransferases and TET enzymes, the cnidarian and ctenophore methylomes are rather static, as it has previously reported for insects, and low levels of genome wide methylation are observed, concentrated in gene bodies. However, the sponge methylome is heavily methylated, showing a methylation profile similar to that of vertebrates. Highly expressed genes have unmethylated promoters, which are CpG dense, resembling vertebrate CpG Islands. Moreover, we find differentially methylated regions that change in a directional manner along development, 50% directly in gene promoters, correlating with changes in gene expression. In contrast, hydroxymethylation does not seem to mark active demethylation in the sponge genome. Overall, our analyses show a clear example of epigenome convergence between sponges and vertebrates, revealing unprecedented plasticity in animal methylomes.