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Abstract Wolbachia is an obligate intracellular α-proteobacterium, which commonly infects arthropods and filarial nematodes. Different strains of Wolbachia are capable of a wide range of regulatory manipulations in their diverse hosts, including the modulation of host cellular differentiation to influence host reproduction. The genetic basis for the majority of these phenotypes is unknown. The wWil strain from the neotropical fruit fly, Drosophila willistoni, exhibits a remarkably high affinity for host germline-derived cells relative to the somatic cells. This trait could be leveraged for understanding how Wolbachia influences the host germline and for controlling host populations in the field. To further the use of this strain in biological and biomedical research, we sequenced the genome of the wWil strain isolated from host cell culture cells. Here, we present the first high quality Nanopore assembly of wWil, the Wolbachia endosymbiont of D. willistoni. Our assembly resulted in a circular genome of 1.27 Mb with a BUSCO completeness score of 99.7%. Consistent with other insect-associated Wolbachia strains, comparative genomic analysis revealed that wWil has a highly mosaic genome relative to the closely related wMel and wAu strains from Drosophila melanogaster and Drosophila simulans, respectively.