A vast array of animal body plans has arisen from a common set of regulatory transcription factor (TF) genes that interact with cis-regulatory sequences known as promoters and enhancers. However, the origin and evolution of enhancers has been thought to be intractable due to their fast evolution. Here, we examine putative enhancers located in conserved syntenic gene units in the sponge Amphimedon queenslandica in transgenic zebrafish assays. Comparison of the sponge enhancers with vertebrate sequences reveals no significant sequence identity. However, we find that the sponge enhancers drive highly cell-type specific expression in fish. Gene expression appeared restricted to neuronal cell subpopulations. Remarkably, reporter expression was associated with the endogenous expression of the fish developmental target gene suggesting that the sponge enhancers contain the necessary regulatory information to drive correct expression in a zebrafish TF-background. Given this, we designed an in silico method to identify enhancer orthologs using a newly developed approach based on the density TF binding motifs. By characterizing TF-binding motif density in the sponge Islet enhancer, we were able to identify its orthologues in human and mouse. Despite the mammalian enhancers lacking primary sequence identity to both the sponge and zebrafish enhancers, they drove very similar reporter gene expression patterns in the zebrafish as the sponge. These results reveal that the origin of deeply conserved developmental enhancers can be traced back to origin of metazoan multicellularity. Despite this deep functional conservation, orthologous enhancers are unrecognizable using standard methods. However, the TF-binding motif density analysis we developed deciphers the regulatory information encapsulated in these enhancers. Together, these results suggest that developmental and cell-type enhancers evolved early in metazoan evolution and have been maintained independently in lineages that diverged over 700 million years ago, and that animal enhancers are as deeply conserved as many metazoan transcription factor families.