Skin coloration is crucial for the survival of animals and ranges from spectacular colorful displays used to attract a mate to cryptic camouflage used to avoid predators. Among the 3 main types of chromatophores, melanophores are the most widespread in vertebrates and can set the skin tone by the amount of melanin they produce and store in dedicated vesicles, the melanosomes. Mutations associated with melanophore differentiation and maturation result in hypomelanistic and amelanistic phenotypes, both extensively studied in mammals but less so in snakes and lizards. Here, we characterize at the genomic, transcriptomic, and histological level, the Hypomelanistic corn snake morph and 3 hypomelanistic leopard gecko morphs. To minimize bias in studying leopard gecko color morphs, we first assembled a chromosome-level genome from a wild-type individual in terms of coloration. We propose that candidate mutations in 3 melanogenesis factors generate these phenotypes: (i) tyrosinase (TYR), an essential enzyme for melanin synthesis, (ii) NCKX5 (SLC24A5), an ion exchanger involved in melanosome maturation, and (iii) the P protein (OCA2), a transmembrane transporter for tyrosine. Our extended bulk RNA sequencing analyses show that additional pigmentation-related genes, affecting melanin production, melanosome motility, and melanophore migration, are dysregulated in the embryonic skin of the mutated animals. This observation highlights the likely associations among the corresponding pathways and is in line with our electron microscopy imaging results. Indeed, the subcellular structure of melanophores is uniquely altered at each of the 4 morphs and likely reflects a multigenic effect. These findings demonstrate that conserved pigmentation genes can produce species-specific effects, underscoring the modular nature of skin coloration in vertebrates. Our work establishes reptiles as comparative models for studying pigment cell biology and reveals evolutionary flexibility in the genetic regulation of melanogenesis.