Colour and pigmentation variation attracted fish biologists for a while, but high-throughput genomic studies investigating the molecular basis of body pigmentation remain still limited to few species and conservation biology issues ignored. Using 75,684 SNPs, we investigated the genomic basis of pigmentation pattern variation among individuals of the Atlantic and Mediterranean clades of the brown trout (Salmo trutta), a polytypic species in which Atlantic hatchery individuals are commonly used to supplement local wild populations. Using redundancy analyses and genome-wide association studies, a set of 384 “colour patterning loci” (CPL) significantly correlated with pigmentation traits such as the number of red and black spots on flanks, but also the presence of a large black stain on the opercular bone was identified. CPLs map onto 35 out of 40 brown trout linkage groups indicating a polygenic basis to pigmentation patterns. They are mostly located in coding regions (43.4%) of 223 candidate genes, and correspond to GO-terms known to be involved in pigmentation (e.g. calcium and ion-binding, cell adhesion). Annotated genes especially include 24 candidates with known pigmentation effects (e.g. SOX10, PEML, SLC45A2), but also the Gap-junction Δ2 (GJD2) gene that was previously showed be differentially expressed in trout skin. Patterns of admixture were found significantly distinct when using either the full SNP data set or the set of CPLs, indicating that pigmentation patterns accessible to practitioners are not a reliable proxy of genome-wide admixture. Consequences for management are discussed.