Invasive species disrupt island ecosystems, posing significant threats to native species. The avian vampire fly (Philornis downsi), introduced into the Galapagos Islands, has become a major threat to endemic birds including Darwins finches, yet the genetic mechanisms of its invasion remain unclear. This study used whole-genome sequencing of P. downsi populations from Galapagos and its native range in mainland Ecuador, revealing reduced genetic diversity in Galapagos, indicative of a recent bottleneck. We found evidence of ongoing gene flow among island populations and identified regions under positive selection near genes related to neural signaling, muscle development, and metabolic processes, which may have contributed to the fly invasion success in Galapagos. These findings highlight the importance of genomic research for mitigating the impact of P. downsi on Galapagos biodiversity.