Free-breeding dogs have occupied the Galápagos Islands at least since the 1830s; however, it was not until the 1900s that dog populations grew substantially, endangering wildlife and spreading disease. In 1981, efforts to control the population size of free-roaming dogs began. Yet, there exist large free-roaming dog populations on the islands of Isabela and Santa Cruz whose ancestry has never been assessed on a genome-wide scale. We thus performed a complete genomic analysis of the current Galápagos dog population, as well as historical Galápagos dogs sampled between 1969 and 2003, testing for population structure, admixture, and shared ancestry. Our dataset included samples from 187 modern and six historical Galápagos dogs, together with whole-genome sequences from over 2,000 modern purebred and village dogs. Our results indicate that modern Galápagos dogs are recently admixed with purebred dogs but show no evidence of a population bottleneck related to the culling. Additionally, identity-by-descent analyses reveal evidence of shared shepherd-dog ancestry in the historical dogs. Overall, our results demonstrate that the 1980s culling of dogs was ineffective in controlling population size and did little to reduce genetic diversity, instead producing a stable and expanding population with genomic signatures of modern purebred dogs. The insights from this study can be used to improve population control strategies for the Galápagos Islands and other endangered endemic communities.