In host-symbiont systems, interspecific transmissions create opportunities for host switches, potentially leading to cophylogenetic incongruence. In contrast, conspecific transmissions often result in high host specificity and congruent cophylogenies. In most bird-feather mite systems, conspecific transmission is considered dominant, while interspecific transmission is supposedly rare. However, while mites typically maintain high host specificity, incongruent cophylogenies are common. To explain this conundrum, we quantify the magnitude of conspecific vs. interspecific transmission in the brood parasitic shiny cowbird (Molothrus bonariensis). M. bonariensis lacks parental care, allowing the assessment of the role of horizontal transmission alone in maintaining host specificity. We found that despite frequent interspecific interactions via foster parental care, mite species dispersing via conspecific horizontal contacts are three times more likely to colonize M. bonariensis than mites transmitted vertically via foster parents. The results highlight the previously underappreciated rate of transmission via horizontal contacts in maintaining host specificity on a microevolutionary scale. On a macroevolutionary scale, however, host switches were estimated to have occurred as frequently as codivergences. This suggests that macroevolutionary patterns resulting from rare events cannot be easily generalized from short-term evolutionary trends.