Development proceeds via the progressive installation of regulatory states that specify and diversify the cells of an embryo. The combination of signaling systems and transcription factors (TFs) required for such processes are encoded in developmental gene regulatory networks (GRN). My thesis research has explored gene regulatory principles governing cell fate decisions using an embryonic cell type called the neural crest. The neural crest is a vertebrate-specific stem cell population that gives rise to several systems including the craniofacial skeleton, the peripheral nervous system, and the pigmentation of the skin. Studies in multiple model organisms have resulted in the assembly of a comprehensive gene regulatory network (GRN) that orchestrates the formation, migration, and differentiation of this cell type. While the current version of the network has expanded our understanding of developmental transitions, it was assembled via a candidate-based approach, which overly emphasizes classical marker genes. Additionally, there remains limited information on the formation of human neural crest cells, despite its importance for the etiology of several pathologies. Motivated by these outstanding questions, my thesis work has aimed to unbiasedly identify novel transcriptional and post-transcriptional regulators of the neural crest using in vitro and in vivo systems. In the first part of my thesis work, I combined a TF-focused CRISPR screen with epigenomic and transcriptional profiling of human neural crest cells to identify novel processes involved in the formation of this cell type. This work demonstrated that the AP-1 TF complex cooperates with the cell-type specific pioneer factor TFAP2A to shape the neural crest epigenome. Furthermore, this work demonstrated that AP-1 serves as a nuclear effector of FGF/MAPK signaling in this cell type, a previously missing link between FGF signaling and neural crest development. Additionally, functional characterization of AP-1 in the chick embryo demonstrated this mechanism is conserved across vertebrates. In the second part of my dissertation research, I aimed to elucidate post-transcriptional mechanisms governing neural crest cell formation. To this end, I investigated the requirement of the miRNA biogenesis enzyme DICER in avian neural crest cells, coupled with small RNA-sequencing. Through this analysis, I identified several miRNAs that collectively target components of the FGF signaling pathway, a central player in the neural crest GRN. Inactivation of this post-transcriptional circuit results in a fate switch, in which neural crest cells are converted into progenitors of the central nervous system. Thus, the post-transcriptional attenuation of signaling systems is a pre-requisite for proper segregation of ectodermal cell types. Taken together, my thesis work has unbiasedly identified epigenetic and post-transcriptional mechanisms controlling FGF signaling in neural crest development.