Understanding how genetic drift and inbreeding can shape phenotypic traits and the expression of rare genetic variants can be important for conservation management in small and isolated populations. Following the recolonization of the grey wolf (Canis lupus) on the Scandinavian peninsula, the population has never exceeded a few hundred wolves and remains semi-isolated from the neighboring wolf populations in Finland and Russia. The population traces back to seven founders and is highly inbred. Inbreeding depression has been demonstrated, including effects on reproductive output and several congenital deformities. Some wolves also show anomalous coat color, characterized by hypopigmentation displayed as white tail tips, or even larger areas of white fur. We used four decades of monitoring data, dating back to the recolonization of the Scandinavian peninsula in 1983, to examine the occurrence of expressed anomalous coat color, investigating its origin and inheritance, genetic architecture, and the effect of inbreeding. SNP genotyping revealed a distinct haplotype linked to the Melanocyte-inducing transcription factor (MITF) gene that co-segregated with anomalous coat color, suggesting a direct causal effect of this variant. The MITF gene regulates mammalian melanocyte development, which in turn affects pigmentation. Our findings demonstrate that the identified gene variant is recessive, which in the homozygous state likely causes the disruption of normal melanocyte development, leading to unpigmented or hypopigmented areas. The origin of this haplotype was traced to the third founder, reproducing for the first time in 1991. Indeed, the genetic constraints and subsequent inbreeding shaped by few founders, small population size, and semi-isolation over several decades point towards the importance of genetic diversity and facilitated gene flow between populations, but also to how such vital immigration can bring about unforeseen side effects if inbreeding continues within the immigrant lineages.