While whole-genome sequencing has been applied extensively to investigate the genetic diversity of global populations, ethnic minority groups in Pakistan are generally underrepresented. In particular, little is known about the genetic origin and highland adaptation of the Pamirian Wakhi people. According to Chinese historical records, the geographical location and language usage of Wakhi may be closely related to Xinjiang Tajiks. In this study, based on high-coverage (∼30×) whole-genome sequencing of eight Wakhi and 25 Xinjiang Tajik individuals, we performed data analyses together with worldwide populations to gain insights into their genetic composition, demography, and adaptive evolution to the highland environment. The Wakhi derived more than 85% of their ancestry from West Eurasian populations (European ∼44.5%, South Asian ∼42.2%) and 10% from East Eurasian populations (Siberian ∼6.0%, East Asian ∼4.3%). Modeling the admixture history of the Wakhi indicated that the early West-East admixture occurred ∼3,875 to 2,250 years ago and that the recent admixture occurred ∼750 to 375 years ago. We identified selection signatures across EGLN3, in particular, a distinctive evolutionary signature was observed, and a certain underlying selected haplotype showed higher frequency (87.5%) in the Wakhi than in nearby Xinjiang Tajiks and other highlanders. Interestingly, we found high-frequency archaic sequences in the Wakhi genome, which overlapped with several genes related to cellular signaling transduction, including MAGI2, previously associated with high-altitude adaptation. Our analysis indicates that the Wakhi are distinct from the Xinjiang Tajiks and Tajikistan Tajiks and sheds light on the Wakhi's ancestral origin and genetic basis of high-altitude adaptation.