Neural crest (NC) is a vertebrate-specific embryonic progenitor cell population at the basis of important vertebrate features such as the craniofacial skeleton and pigmentation patterns. Despite the wide-ranging variation of NC-derived traits across vertebrates, the contribution of NC to species diversification remains largely unexplored. Here, leveraging the adaptive diversity of African Great Lakes' cichlid species, we combined comparative transcriptomics and population genomics to investigate the evolution of the NC genetic programme in the context of their morphological divergence. Our analysis revealed substantial differences in transcriptional landscapes across somitogenesis, an embryonic period coinciding with NC development and migration. This included dozens of genes with described functions in the vertebrate NC gene regulatory network, several of which showed signatures of positive selection. Among candidate genes showing between-species expression divergence, we focused on two teleost-specific paralogs of the NC-specifier gene sox10 ( sox10a and sox10b ) as prime candidates to influence NC development. These genes, expressed in NC cells, displayed remarkable spatio-temporal expression variation in cichlids, suggesting their contribution to inter-specific morphological differences. Finally, through CRISPR/Cas9 mutagenesis, we experimentally demonstrated the functional divergence between cichlid sox10 paralogs, with the acquisition of a novel skeletogenic function by sox10a . When compared to the two teleost models zebrafish and medaka, our findings reveal that sox10 duplication, although retained in most teleost lineages, have had variable functional fates across their phylogeny. Altogether, our study suggests that NC-related processes - particularly those controlled by sox10 s - might be involved in generating morphological diversification between species and lays the groundwork for further investigations into the mechanisms underpinning vertebrate NC diversification.