Loss of pigmentation is a hallmark of domestication, and dogs offer a unique model for understanding the genetics of fur coloration. The aim of this study was to use dense genetic mapping to map loci underlying variations in color and whiteness in a population of laboratory beagles. A total of 190 beagles with well-defined pedigrees were phenotyped for the amount of white color in six different body parts, including the saddle. All individuals were genotyped on 85,172 informative and valid SNP-markers and the genome-wide associations for the amount of white in each body part were determined. There was a large variation in the amount of white on different parts of the body, and the whiteness was highly correlated within individuals, except for saddle color which was only moderately correlated with overall whiteness. The GWAS showed significant associations with two loci, one on chromosome 5, containing the MC1R gene, and one on chromosome 20, containing the MITF gene. Our results suggest that the variation in loss of pigmentation is largely a function of regulatory variation related to these genes.