Species are often composed of evolutionarily distinct populations and lineages. Deciphering the evolutionary history of recently diverged species with multiple lineages remains challenging because genealogical discordance is common across the genome. Emerging genomic and statistical tools are allowing unprecedented insight into the evolutionary history of complicated species that have been notoriously difficult to resolve. The gray wolf exemplifies this challenge as it has multiple recognized lineages and has only recently diverged from other canids. In this dissertation, I use genome-wide data to study the evolutionary history of gray wolves in Eurasia, with a focus on investigating the phylogenomics, demographic history, and role of adaptive introgression. For my first chapter, I investigate the genomic distinctiveness of wolves corresponding to two deeply divergent mitochondrial clades restricted to the Indian subcontinent and the Tibetan plateau, respectively. Using the first whole genome sequences of four Indian wolves along with those of two newly sequenced Tibetan wolves and 31 additional canids, I demonstrate Indian and Tibetan wolves are the two most deeply divergent wolf lineages and highly distinct from broadly distributed wolf populations corresponding to the mitochondrial Holarctic clade. Low-recombination regions of the genome provided evidence that the Indian wolf is the most basal wolf lineage, in contrast to the mitochondrial DNA, showing the Tibetan wolf as the most basal lineage. Our findings imply that southern regions of Asia have been important centers for gray wolf evolution and that the Indian wolf represents one of the world’s most endangered and evolutionarily distinct wolf lineages. My second chapter focuses on distinguishing secondary contact zones and investigating adaptive introgression among wolf lineages in Asia. I used 5 newly and 7 recently sequenced wolf (Canis lupus) genomes from the lowland plains and high-altitude mountains of Pakistan, India, and Kyrgyzstan, along with 79 additional canid genomes, to explore the possibility that adaptive introgression from specialized basal wolf lineages into Holarctic wolves facilitated their range expansion. I detected three narrow secondary contact zones among the widespread Holarctic lineage and the divergent Indian and Tibetan lineages. Within West-Asian Holarctic wolves, I detected several gene regions that were highly differentiated compared to other Holarctic wolves and signals of higher-than expected levels of introgression from Indian or African wolves. Additionally, in the high-altitude Central Asian wolf, I found similar evidence for adaptive introgression from the Tibetan wolf including gene related to hypoxia adaptation in other mammals. Lastly, demographic analyses revealed Indian and Tibetan wolf lineages were likely isolated within separate glacial refugia in Asia while the Holarctic lineage underwent massive expansion events during the late Pleistocene. In Chapter 3, I use genome-wide data from 5 newly sequenced gray wolves from Pakistan to more robustly investigate the locations of secondary contact zones and admixture among the three wolf lineages at these contact zones. Using a total of 8 wolves from Pakistan and an additional 48 canids, clustering and admixture analyses indicated high proportions of Indian ancestry was present in the lowlands of the Indus plains, Potwar plateau, and Western mountain ranges of Pakistan. Except for small amounts of Tibetan ancestry detected in two wolves from the Karakoram Mountains of northern Pakistan, the Tibetan lineage appeared to end to the east in the Ladakh region of India. These findings clarify the boundaries of the three divergent wolf lineages and highlight the conservation significance of Pakistan’s wolf populations, especially the wolves in Sindh and Punjab that represent the Indian lineage. Overall, this dissertation provides insight into the evolutionary and historical processes that shape genomic divergence and local adaptation in a wild and highly mobile species.