Abstract Invasive species pose significant threats to island ecosystems, often leading to the decline of native species and the disruption of ecological balance. The avian vampire fly (Philornis downsi), introduced to the Galápagos Islands of Ecuador, has emerged as a major threat to the endemic avifauna, parasitizing multiple species of Darwin's finches and other passerines. Yet, the genetic mechanisms of its invasion remain unclear. In this study, we conducted the first whole-genome sequencing analysis of P. downsi populations from the Galápagos Islands and their native range in mainland Ecuador. Our results reveal genomic signatures of a founder effect, with reduced genetic diversity in the Galápagos populations, indicative of a recent population bottleneck. We found a lack of significant genetic differentiation and evidence of ongoing gene flow among island populations. Despite low genetic diversity in island populations, we identified adaptive genetic changes, including regions possibly under positive selection near genes related to neural signaling, muscle development, and metabolic processes, which may have contributed to the fly's invasion success. Additionally, we uncovered genetic changes associated with precipitation-related climate adaptation, highlighting the possible role of environmental factors in shaping genetic variation in P. downsi. Our findings provide crucial insights into the invasion dynamics of P. downsi in Galápagos, emphasizing the importance of genomic research in informing conservation strategies. The identification of key adaptive genomic loci and potential environmental drivers of genetic change will aid in the development of targeted management practices to mitigate the impact of this invasive species on the unique biodiversity of the Galápagos Islands.