The invasive avian vampire fly (Philornis downsi) is considered one of the greatest threats to the unique and endemic avifauna of the Galpagos Islands, Ecuador. The fly parasitizes nearly every passerine species, including Darwins finches, in the Galpagos. The fly is thought to have been introduced from mainland Ecuador, although the full pathway of invasion is not yet known. The majority of research to date has focused on the effects of the fly on the fitness of avian hosts and explorations of mitigation methods. A lag in research related to the genetics of this invasion demonstrates, in part, a need to develop full-scale genomic resources with which to address further questions within this system. In this study, an adult P. downsi collected from San Cristobal Island within the Galpagos archipelago was sequenced to generate a high-quality genome assembly. We examined various features of the genome (e.g., coding regions, non-coding transposable elements) and carried out comparative genomics analysis against other dipteran genomes. We identified lists of gene families that are significantly expanding/contracting in P. downsi >that are related to insecticide resistance, detoxification, and potential feeding ecology and counter defense against host immune responses. The P. downsi genome assembly provides an important foundational resource for studying the molecular basis of its successful invasion in the Galpagos and the dynamics of its population across multiple islands. The findings of significantly changing gene families associated with insecticide resistance and immune responses highlight the need for further investigations into the role of different gene families in aiding the flys successful invasion. Furthermore, this genomic resource will also better help inform future research studies and mitigation strategies aimed at minimizing the flys impact on the birds of the Galpagos.