Inherited symbionts are important drivers of arthropod evolutionary ecology, with microbes acting both as partners that contribute to host adaptation, and as subtle parasites that drive host evolution. New symbioses are most commonly formed through lateral transfer, where a microbial symbiont passes infectiously from one host species to another, and then spreads through its new host population. However, the rate of horizontal transfer has been regarded as sufficiently low that population and coevolutionary processes can be approximated to one, where the symbiont interacts with a single host species. In this paper, we demonstrate experimentally that horizontal transfer of the son-killer infection of Nasonia wasps occurs readily following multi-parasitism events (two species of parasitoid wasp sharing a fly pupal host), and provide phylogenetic evidence of recent and likely ongoing transmission amongst members of the community of wasps utilizing filth flies. Combining per contact transmission rates estimated in the laboratory with rates of multiparasitism in the field produces an estimate that an infected Nasonia vitripennis individual in an Eastern US bird's nest habitat has a 12% chance of passing the infection into N. giraulti. We conclude that the single host-single symbiont framework is therefore insufficient for understanding the population and evolutionary dynamics in this system and caution against blind acceptance of the single host/single symbiont framework. We conjecture that lateral transfer rates that require a multi-host framework will most likely be seen in symbionts that retain the ability to cross host epithelia, and that this will be correlated to the recency with which the symbionts have been free living.