Insect diversification is thought to have been catalyzed by widespread specialization on novel hosts—a process underlying exceptional radiations of phytophagous beetles, lepidopterans, parasitoid wasps, and inordinate lineages of symbionts, predators, and other trophic specialists. The fidelity of such interspecies partnerships is often posited to arise from sensory tuning to host-derived cues, a model supported by studies of neural function in host-specific model species. Abundant literature on parasites also suggest that extrinsic factors, namely dispersal mechanisms and aggressiveness/acceptance from novel hosts, externally enforces host specificity. Here, I first review what is known about host specificity, why it arises and how it is controlled, and then explore how these factors influence the biology of myrmecophiles, the intimate symbiotic associates of ants. I then test the mechanisms of host specificity by investigating the chemosensory basis of symbiotic interactions between a myrmecophile rove beetle and its single, natural host ant species. I show that host cues trigger analogous behaviors in both the ant and myrmecophile. Cuticular hydrocarbons—the ant's nestmate recognition pheromones—elicit partner recognition in the myrmecophile and execution of ant grooming behavior that achieves chemical mimicry. The myrmecophile also follows host trail pheromones, permitting inter-colony dispersal. Remarkably, however, the myrmecophile performs these same adaptive behaviors with non-host ants separated by up to ~100-million years and shows minimal preference for its natural host over non-host ant species. Experimentally validated agent-based modelling supports a scenario in which specificity is enforced by physiological constraints on dispersal, and negative fitness interactions with alternative hosts, rather than via sensory tuning. Infrequent realization of latent compatibilities of specialists with alternative hosts may facilitate host switching, and the persistence and diversification of seemingly specialized clades over deep time.