The ability of vector-borne diseases to persist and spread is closely linked to the ecological characteristics of the vector species they use. Yet there have been no investigations of how species used as vectors by pathogens such as the plague bacterium differ from closely related species that are not used as vectors. The plague bacterium uses mammals as reservoir hosts and fleas as vectors. The ability of different fleas to serve as vectors is assumed to depend on how likely they are to experience gut blockage following bacterial multiplication; the blockage causes fleas to regurgitate blood into a wound and thus inject bacteria into new hosts. Beyond these physiological differences, it is unclear whether there exist fundamental ecological differences between fleas that are effective vectors and those that are not. Here, using a comparative analysis, we identify clear associations between the ability of flea species to transmit plague and their ecological characteristics. First, there is a positive relationship between the abundance of flea species on their hosts and their potential as vectors. Second, although the number of host species exploited by a flea is not associated with its potential as a vector, there is a negative relationship between the ability of fleas to transmit plague and the taxonomic diversity of their host spectrum. This suggests a correlation between some ecological characteristics of fleas and their ability to develop the plague blockage. The plague pathogen thus uses mainly abundant fleas specialized on a narrow taxonomic range of mammals, features that should maximize the persistence of the disease in the face of high flea mortality, and its transmission to suitable hosts only. This previously unrecognized pattern of vector use is of importance for the persistence and transmission of the disease.