The gallinae complex of the genus Dermanyssus comprises blood-feeding mite species associated with birds. Their host range varies widely, from highly generalist (birds belonging to 9 different orders) to highly specialized (exclusively the rock pigeon, Columba livia). Interestingly, a sharp ecological segregation separates these two extremes: the generalist species is never found on pigeons—the only known host of the specialist species—while pigeons are frequently found in sympatry or even syntopy with several of its host species. And paradoxically, while the generalist species poses a problem in poultry farming, the specialist species is the one that most often bites humans. Unraveling the evolutionary ecology of these ectoparasites would advance our understanding of fundamental biological principles, but also lay the groundwork for essential knowledge to better manage their interactions with humans (damage in egg-laying poultry farms, human bites in urban environments). Combes’ encounter and compatibility filter paradigm regarding host specificity proposes four scenarios leading to the success or failure of a potential host-parasite interaction. Here, we will distinguish within the encounter filter an ecological component (shared microhabitat) and a recognition component (physico-chemical interactions). The objective of this study is to determine to what extent the recognition encounter filter and the compatibility filter explain the current distribution of these species. METHODS. To do this, we conducted laboratory experiments allowing for the artificial opening of the ecological encounter filter at two scales: individual responses to direct exposure to a chicken or pigeon under controlled conditions (feeding rate, mortality, molting, egg-laying), and population growth on chickens or pigeons in closed mesocosms. RESULTS. At the individual level, both species are capable of feeding on both hosts, although with an effect of the recognition encounter filter (feeding rates significantly lower on non-hosts). Our results also show a significant effect of the compatibility filter, with reduced molting rates and reduced numbers of eggs laid after feeding on non-hosts compared to the preferred host in both species. At the population level, the failure of development on non-hosts in both species in mesocosms confirms a strong effect of combined filters even in the absence of competitive exclusion.