Vertebrate genomes are generally depleted of CpG dinucleotides. This overall depletion of CpG dyads is primarily due to a higher mutation rate of CpG > TpG, caused by frequent methylation of cytosine in the CpG context (5mCG). In contrast, regions known as CpG islands (CGIs) exhibit a notably higher CpG content. This phenomenon is typically attributed to lower rates of CpG > TpG substitutions in CGIs, which is a consequence of low 5mCG levels at these sequences. CGIs frequently coincide with vertebrate gene promoters, and less frequently enhancers, rendering both element classes sensitive to 5mCG – mediated inactivation. CGIs have thus predominantly been studied in the context of hypermethylated vertebrate genomes, however it is currently unclear to what extent genome-wide hypermethylation observed in vertebrates contributed to CGI formation. Unlike vertebrate genomes, non-vertebrate genomes are typically sparsely methylated, thus the possibility of CGI existence in non-vertebrate lineages has not been greatly considered. To interrogate the existence of non-methylated CGI-like sequences across metazoans, we sequenced CpG-rich fractions of eight diverse genomes containing varying levels of 5mCG. Analysis of these non-vertebrate CpG-rich sequences revealed vertebrate CGI-like DNA and chromatin features, including CpG and GC richness, DNA hypomethylation, transcription factor binding motifs, accessible chromatin, and enrichment of active histone marks H3K4me3 and H3K27ac. The identification of CGI-like regulatory sequences in non-vertebrate metazoans thus challenges the long-standing assumption of the importance of 5mCG in CGI formation, providing valuable insights into the fundamental mechanisms controlling gene expression.