Throughout most of the Americas, post-colonial dogs largely erased the genetic signatures of pre-historical dogs. However, the North American Arctic harbors dogs that are potentially descended from pre-historical ancestors, as well as those affected by post-colonial translocations and admixtures. In particular, Inuit dogs from Canada and Greenland are thought to descend from dogs associated with Thule peoples, who relied on them for transportation ca. 1000 years ago. Whether Thule dogs reflected an earlier colonization by Paleoeskimo dogs ca. 4500 years ago is unknown. During the Alaskan Gold Rush, additional sled dogs, possibly of post-colonial derivation, the Alaskan Husky, Malamute and Siberian Husky, were used in the Arctic. The genealogical relationships among and origins of these breeds are unknown. Here we use autosomal, paternal and maternal DNA markers to (1) test the hypothesis that Inuit dogs have retained their indigenous ancestry, (2) characterize their relationship to one another and to other Arctic breeds, and (3) estimate the age of North American indigenous matrilines and patrilines. On the basis of the agreement of all three markers we determined that Inuit dogs have maintained their indigenous nature, and that they likely derive from Thule dogs. In addition, we provide support for previous research that the Inuit dogs from Canada and Greenland dog should not be distinguished as two breeds. The Alaskan Husky displayed evidence of European introgression, in contrast to the Malamute and Siberian Husky, which appear to have maintained most of their ancient Siberian ancestry.