A dynamic continuum exists from free-living environmental microbes to strict host-associated symbionts that are vertically inherited. However, knowledge of the forces that drive transitions in symbiotic lifestyle and transmission mode is lacking. *Arsenophonus* is a diverse clade of bacterial symbionts, comprising reproductive parasites to coevolving obligate mutualists, in which the predominant mode of transmission is vertical. We describe a symbiosis between a member of the genus *Arsenophonus* and the Western honey bee. The symbiont shares common genomic and predicted metabolic properties with the male-killing symbiont *Arsenophonus nasaniae*, however we present multiple lines of evidence that the bee *Arsenophonus* deviates from a heritable model of transmission. Field sampling uncovered spatial and seasonal dynamics in symbiont prevalence, and rapid infection loss events were observed in field colonies and laboratory individuals. Fluorescent in situ hybridisation showed *Arsenophonus* localised in the gut, and detection was rare in screens of early honey bee life stages. We directly show horizontal transmission of *Arsenophonus* between bees under varying social conditions. We conclude that honey bees acquire *Arsenophonus* through a combination of environmental exposure and social contacts. These findings uncover a key link in the *Arsenophonus* clade’s trajectory from free-living ancestral to obligatory mutualism, and provide a foundation for studying transitions in symbiotic lifestyle.

Georgia C. Drew, Giles E. Budge, Crystal L. Frost, Peter Neumann, Stefanos Siozios, Orlando Yañez, Gregory D. D. Hurst