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Fine-mapping and melanocyte expression data collectively suggest two potential causal genes with opposite association with risk: higher levels of Rap guanine nucleotide exchange factor 1 (                   <jats:italic>RAPGEF1</jats:italic>                   ) and lower levels of uridine-cytidine kinase 1 (                   <jats:italic>UCK1</jats:italic>                   ). Colocalization analyses and conditional TWAS suggest multiple causal                   <jats:italic>cis</jats:italic>                   -regulatory sequence variants in partial linkage disequilibrium (LD) to each other. Melanocyte capture-HiC and CRISPR-inhibition demonstrated regulatory interactions between fine-mapped variants and the                   <jats:italic>RAPGEF1</jats:italic>                   and                   <jats:italic>UCK1</jats:italic>                   promoters. Focusing on                   <jats:italic>RAPGEF1</jats:italic>                   , we demonstrate                   <jats:italic>RAPGEF1</jats:italic>                   expression promotes melanocyte growth and drives malignant transformation of human immortalized melanocytes. Following treatment with human EGF,                   <jats:italic>RAPGEF1</jats:italic>                   overexpression activated both RAP1 and RAS. Further, we show                   <jats:italic>RAPGEF1</jats:italic>                   expression is significantly enriched in melanomas lacking strongly activating RAS-MAPK mutations, suggesting that                   <jats:italic>RAPGEF1</jats:italic>                   may promote oncogenic RAS-MAPK signaling in melanomas. Furthermore, in these tumors, we provide preliminary evidence to support the prognostic relevance of                   <jats:italic>RAPGEF1</jats:italic>                   expression in patients lacking                   <jats:italic>RAS</jats:italic>                   or                   <jats:italic>BRAF</jats:italic>                   mutations. Together with other recent studies, these data suggest that germline variation influencing RAS activation may play a key role in nevus development and melanoma risk.                 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