Coevolutionary associations between hosts and symbionts (or parasites) are often reflected in correlated patterns of divergence as a consequence of limitations on dispersal and establishment on new hosts. Here we show that a phylogenetic correlation is observed between chaetodactylid mites and their hosts, the long-tongued bees; however, this association manifests itself in an atypical fashion. Recently derived mites tend to be associated with basal bee lineages, and vice versa, ruling out a process of cospeciation, and the existence of mites on multiple hosts also suggests ample opportunity for host shifts. An extensive survey of museum collections reveals a pattern of infrequent host shifts at a higher taxonomic level, and yet, frequent shifts at a lower level, which suggests that ecological constraints structure the coevolutionary history of the mites and bees. Certain bee traits, particularly aspects of their nesting behavior, provide a highly predictive framework for the observed pattern of host use, with 82.1% of taxa correctly classified. Thus, the museum survey and phylogenetic analyses provide a unique window into the central role ecology plays in this coevolutionary association. This role is apparent from two different perspectives—as (a) a constraining force evident in the historical processes underlying the significant correlation between the mite and bee phylogenies, as well as (b) by the highly nonrandom composition of bee taxa that serve as hosts to chaetodactylid mites.