DNA methylation has been found throughout animal kingdom, but it is still unclear whether this epigenetic mechanism affects the evolution of genomic elements in animals. Here, we compare the DNA methylomes of gametes and embryos from 7 representative animal species. We find that parental methylomes are propagated to the progeny without significant changes during embryogenesis in cnidarians and insects, but undergo substantial reprogramming in echinoderms, and the reprogramming become more dramatic during deuterostome evolution. Interestingly, young gene promoters in mammals tend to be reprogrammed, usually have low CpG density, don’t contain CpG Islands (CGIs) and are hypermethylated, and the hypermethylated status correlates to lower transcription. Unexpectedly, an evolutionary trend of CpG accumulation in promoters is observed only during vertebrate evolution. Most of ancient gene promoters in mammals form CGIs, which are generally unmethylated and associate with higher transcription. Thus, to gain unmethylated pattern to facilitate transcription, nature selection should be in favor of the formation of CGIs in promoters. Our data suggest that the formation of CGIs in promoters is driven by DNA methylation during mammalian evolution. Overall design: MethylC-seq were performed with gametes and early developmental embryos in four species, including honey bee, sea anemone, sea urchin and ciona. We compared the inheritance and programming of parental CpG methylation of animal species including cnidarian, protostome and deuterostome.