Updated project metadata. The assembly of the neuronal and other major cell type programs occurred early in animal evolution. We can reconstruct this process by studying non-bilaterians like placozoans. These small disc-shaped animals have only nine morphologically described cell types and no neurons, but show coordinated behaviors triggered by peptide-secreting cells. We investigated the possible neuronal affinities of these peptidergic cells using phylogenetics, chromatin profiling, and comparative single-cell genomics in four placozoans species. We found highly conserved cell type expression programs across placozoans, including populations of transdifferentiating and cycling cells suggestive of active cell type homeostasis. We also uncovered an unexpected diversity of fourteen peptidergic cell types that express neuronal-associated components like the presynaptic scaffold and that derive from progenitor cells with neurogenesis signatures. In contrast, earlier-branching animals like sponges and ctenophores lacked this conserved expression. Our findings indicate that key neuronal developmental and effector gene modules evolved before the advent of cnidarian/bilaterian neurons in the context of paracrine cell signalling.