AbstractDrosophila suzukiirecently invaded North America and Europe. Populations in Hawaii, California, New York and Nova Scotia are polymorphic forWolbachia, typically with <20% infection frequency. TheWolbachiainD. suzukii, denotedwSuz, is closely related towRi, the variant prevalent in continental populations ofD. simulans.wSuz is also nearly identical toWolbachiafound inD. subpulchrella, plausiblyD. suzukii's sister species. This suggests verticalWolbachiatransmission through cladogenesis (‘cladogenic transmission’). The widespread occurrence of 7–20% infection frequencies indicates a stable polymorphism.wSuz is imperfectly maternally transmitted, with wild infected females producing on average 5–10% uninfected progeny. As expected from its low frequency,wSuz produces no cytoplasmic incompatibility (CI), that is, no increased embryo mortality when infected males mate with uninfected females, and no appreciable sex‐ratio distortion. The persistence ofwSuz despite imperfect maternal transmission suggests positive fitness effects. Assuming a balance between selection and imperfect transmission, we expect a fitness advantage on the order of 20%. Unexpectedly,Wolbachia‐infected females produce fewer progeny than do uninfected females. We do not yet understand the maintenance ofwSuz inD. suzukii. The absence of detectable CI inD. suzukiiandD. subpulchrellamakes it unlikely that CI‐based mechanisms could be used to control this species without transinfection using novelWolbachia. Contrary to their reputation as horizontally transmitted reproductive parasites, manyWolbachiainfections are acquired through introgression or cladogenesis and many cause no appreciable reproductive manipulation. Such infections, likely to be mutualistic, may be central to understanding the pervasiveness ofWolbachiaamong arthropods.