Tephritid fruit flies are important invasive species of ripening fruit and vegetables. Among these include the olive fly (Bactrocera oleae), a globally distributed specialist pest of olives. A component to the olive fly’s adaptation and success as a specialist involves a symbiotic relationship with the gut bacterium Candidatus Erwinia dacicola. The symbiotic relationship with Ca. E. dacicola is unique among studied tephritid fruit flies, as it lives in the digestive tract and has a relatively large genome, but is characteristic of obligate symbionts (e.g., unculturable, being the sole microbial association with the host, and causes a reduction in host fitness when cured). While sequencing the olive fly genome with HiFi and Hi-C sequencing, we obtained a Ca. E. dacicola genome in tandem. Our goals were to uncover the host-microbe dialogues from a genomic perspective to better illuminate why Ca. E. dacicola is an obligate, unculturable bacteria and how it is integrating with the host. In total, 4,675 genes were annotated, but 1783 (38.13%) of these were classified as pseudogenes. Some pathways are complete; those associated with amino acid and vitamin metabolism. Pathways with high pseudogenization rates suggest Ca. E. dacicola have impaired functions in generalized metabolism, carbon utilization, pathogenicity, and signaling systems in relation environmental responses. Our interrogation of the Ca. E. dacicola genome indicates that main service likely provided to the host is the production of amino acids, and the high pseudogenization rate implies the incipient erosion of a formerly free-living