Embryogenesis is characterized by the formation of a complex multicellular organism from a single pluripotent cell. My thesis research has explored this phenomenon through the lens of an embryonic cell population called the neural crest. Neural crest cells are a vertebrate-specific cell type that gives rise to a diverse cell lineage in the developing embryo. The neural crest is postulated to serve as a key driver of vertebrate evolution, contributing to a number of structures in the adult body plan, including the peripheral nervous system, the pigmentation of the skin, and the craniofacial skeleton. Neural crest cell fate commitment requires not only shifts in gene expression, but also an extensive remodeling of the epigenomic landscape. Even so, we still have a superficial understanding of the epigenetic mechanisms which promote neural crest identity. To examine the cis-regulatory landscape of neural crest development, I have coupled both classical embryology approaches and genomic techniques to explore cell state changes underlying neural crest identity. To determine how chromatin states are reorganized during neural crest formation, I examined the function of pioneer factor TFAP2A at discrete stages of development. Through this work, I characterized a mechanism by which TFAP2A remodels the epigenome to allow for progressive cell fate commitment within the neural crest lineage. Next, I aimed to understand the epigenetic basis of neural crest developmental plasticity by performing a cis-regulatory comparison between two neural crest subpopulations, the cranial and trunk neural crest. This allowed me to identify TGF-_ signaling as a potent regulator of cranial neural crest identity. Lastly, I sought to determine how the cis-regulatory landscape is modulated in neural crest cells of different species to give rise to evolutionary novelty. As the craniofacial skeleton is largely derived from the neural crest, I investigated the epigenetic mechanisms driving interspecific variation in beak morphology during avian embryonic development. By performing single-cell ATAC-seq in neural crest cells isolated from three avian species, chicken, quail and duck, I identified conserved cis-regulatory regions displaying species-specific accessibility and discovered a potential role for homeodomain transcription factors in modulating the neural crest epigenetic landscape across species. Together, these studies highlight how the epigenome shapes various aspects of cellular identity throughout development and evolution.