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Coyotes are ubiquitous on the North American landscape as a result of their recent expansion across the continent. They have been documented in the heart of some of the most urbanized cities, such as Chicago, Los Angeles, and New York City. Here, we explored the genomic composition of 16 coyotes in the New York metropolitan area to investigate genomic demography and admixture for urban-dwelling canids in Queens County, New York. We identified moderate-to-high estimates of relatedness among coyotes living in Queens (r = 0.0–0.5) and adjacent neighborhoods, suggestive of a relatively small population. Although we found low background levels of domestic-dog ancestry across most coyotes in our sample (5%), we identified a male suspected to be a first-generation coyote–dog hybrid with 46% dog ancestry, as well as his two putative backcrossed offspring that carried approximately 25% dog ancestry. The male coyote–dog hybrid and one backcrossed offspring each carried two transposable element insertions that are associated with human-directed hypersociability in dogs and gray wolves. An additional, unrelated coyote with little dog ancestry also carried two of these insertions. These genetic patterns suggest that gene flow from domestic dogs may become an increasingly important consideration as coyotes continue to inhabit metropolitan regions.