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Significance New Guinea singing dogs (NGSD) are distinctive among the Canidae because of their unique and characteristic vocalization, isolated habitat, and status as a rare representative of wild dogs. Their scarcity, combined with the knowledge that none have been captured or exported since the late 1970s, supports the hypothesis that NGSD are extinct in the wild. We have analyzed the nuclear genome of the first dogs captured from the highlands of Papua in approximately 50 y. We provide DNA-based evidence for an ancestral relationship between highland wild dogs (HWD) and captive NGSD suggesting that the founding population of the NGSD is not, in fact, extinct and that HWD should be resourced for conservation efforts to rebuild this unique canid population., New Guinea singing dogs (NGSD) are identifiable by their namesake vocalizations, which are unlike any other canid population. Their novel behaviors and potential singular origin during dog domestication make them an attractive, but elusive, subject for evolutionary and conservation study. Although once plentiful on the island of New Guinea (NG), they were presumed to currently exist only in captivity. This conclusion was based on the lack of sightings in the lowlands of the island and the concurrent expansion of European- and Asian-derived dogs. We have analyzed the first nuclear genomes from a canid population discovered during a recent expedition to the highlands of NG. The extreme altitude (>4,000 m) of the highland wild dogs’ (HWD) observed range and confirmed vocalizations indicate their potential to be a wild NGSD population. Comparison of single-nucleotide polymorphism genotypes shows strong similarity between HWD and the homogeneous captive NGSD, with the HWD showing significantly higher genetic diversity. Admixture analyses and estimation of shared haplotypes with phylogenetically diverse populations also indicates the HWD is a novel population within the distinct evolutionary lineage of Oceanic canids. Taken together, these data indicate the HWD possesses a distinct potential to aid in the conservation of NGSD both in the wild and under human care.