BACKGROUND: Advancing our knowledge of vector species genomes is a key step in our battle against the spread of diseases. Biting midges of the genus Culicoides are vectors of arboviruses that significantly affect livestock worldwide. Culicoides stellifer is a suspected vector with a wide range distribution in North America, for which cryptic diversity has been described. RESULTS: With just one specimen of C. stellifer, we assembled and annotated the nuclear and mitochondrial genome using the ultra-low input DNA PacBio protocol. The genome assembly is 119 Mb in length with a contig N50 value of 479.3 kb, contains 11% repeat sequences and 18,895 annotated protein-coding genes. To further elucidate the role of this species as a vector, we provide genomic evidence of a non-retroviral endogenous viral element integrated into the genome that corresponds to rhabdovirus nucleocapsid proteins, the same family as the vesicular stomatitis virus. CONCLUSIONS: This genomic information will pave the way for future investigations into this species's putative vector role. We also demonstrate the practicability of completing genomic studies in small dipterans using single specimens preserved in ethanol as well as introduce a workflow for data analysis that considers the challenges of insect genome assembly.