Animals capable of whole-body regeneration have been studied to understand mechanisms governing the replacement of missing cell types and tissues, including the myriad of cell types within the nervous system. A majority of this work has been performed utilizing the regenerative capacity of these organisms, focusing on postembryonic life-history stages. While uncovering the molecular mechanisms governing the regeneration of specific neural cell types has been extremely informative, very few species capable of whole-body regeneration have accessible embryos that allow for the functional comparison between developmental and regenerative processes with regards to the specification of neural populations. Using the acoel Hofstenia miamia, a member of an early diverging bilaterian lineage that is capable of robust regeneration with manipulable embryos, we sought to determine whether terminally differentiated neural cell types are governed by the same transcriptional programs during both development and regeneration. Utilizing single-cell RNA sequencing (scRNAseq) data collected during development and regeneration, we inferred putative differentiation trajectories of neural cell types. Within these differentiation trajectories, we identified candidate transcription factors that govern the transition to differentiated neural populations. We validated these markers during development and regeneration using fluorescent in situ hybridization and performed RNAi to determine the functions of these transcription factors during each process. This work compares transcriptional regulation of neural cell type specification during development and regeneration as well as the evolution of these processes.