There is arguably no other North American species that better illustrates the complexities of the human-wildlife interface than the coyote. In this study, a melanistic coyote in metropolitan Atlanta, Georgia was exhibiting unusually bold behaviors that included encounters with humans, domestic dogs, and attempts to enter homes. After tracking this coyote (nicknamed Carmine) across a highly urbanized landscape with participatory science, including at least 80 publicly reported sightings, he was captured and relocated to a wildlife sanctuary. Genome-wide analyses revealed 92.8% coyote ancestry, 1.7% gray wolf ancestry, and 5.5% domestic dog ancestry. The dog alleles in Carmine’s genome were estimated to have been acquired by his ancestors 14–29 years ago. Despite his bold behavior, Carmine did not carry any mutations known to shape hypersociability in canines. He did, however, carry a single copy of the dominant mutation responsible for his melanistic coat color. This detailed study of Carmine dispels common assumptions about the reticent coyote personality and the origins of behavior. His unusual bold behavior created a higher level of human-coyote interaction. He now serves as a public ambassador for human-wildlife coexistence, urging the global community to reconsider mythologies about wildlife and promote coexistence with them in landscapes significantly altered by human activity in our rapidly changing world.