Disruption of the transcription factor network governing melanocyte differentiation contributes to the pathogenesis of pigmentation disorders and melanoma. While this network is well-studied, many details are unresolved. Transcription factor activator protein 2 alpha (TFAP2A) is expressed in melanoblasts and mutations in this gene cause pigmentation phenotypes in humans, mice, and zebrafish. However, the the transcriptional targets of TFAP2A, and the extent to which they are shared with MITF, a master regulator of melanocyte biology and melanoma progression, have been unclear. To determine the position of TFAP2A in the melanocyte gene regulatory network, we used microarray analysis in zebrafish and mouse immortalized melanocytes (melan-a cells) to profile genes that are downregulated in the absence of TFAP2A. We then conducted anti-TFAP2A ChIP-seq to create profiles of TFAP2A-bound loci in melan-a cells and human primary melanocytes. Genes at the intersection of the microarray and ChIP-seq profiles are likely direct targets of TFAP2A. These include mc1r and several melanin synthesis or melanosome structural genes, most of which are also thought to be direct targets of MITF. Comparison of our TFAP2A ChIP-seq profile with a published MITF ChIP-seq profile showed that TFAP2A peaks overlap MITF peaks at a large fraction of promoters and enhancers active in these cells. In reporter assays, deletion of TFAP2A binding sites decreased activity of a minimal TRPM1 promoter, similar to published results for deletion of MITF binding sites from this element. Furthermore, counts of embryonic melanocytes indicate a genetic interaction between tfap2a and mitfa in zebrafish. The significance of these findings is, first, they show that TFAP2A and MITF work in parallel to promote gene expression in melanocytes. Second, they show that a widely-expressed transcription factor, TFAP2A, cooperates with a more tissue-restricted transcription factor, MITF, to directly regulate expression of lineage-specific melanocyte genes. Third, they indicate that the reduction of TFAP2A expression levels observed in advanced melanoma is a cause and not an effect of melanoma progression, as such a reduction would be expected to decrease the pro-differentiation effect mediated by TFAP2A.