Animal species with larger local populations tend to be widespread across many localities, whereas species with smaller local populations occur in fewer localities. This pattern is well documented for free‐living species and can be explained by the resource breadth hypothesis: the attributes that enable a species to exploit a diversity of resources allow it to attain a broad distribution and high local density. In contrast, for parasitic organisms, the trade‐off hypothesis predicts that parasites exploiting many host species will achieve lower mean abundance on those hosts than more host‐specific parasites because of the costs of adaptations against multiple defense systems. We test these alternative hypotheses with data on host specificity and abundance of fleas parasitic on small mammals from 20 different regions. Our analyses controlled for phylogenetic influences, differences in host body surface area, and sampling effort. In most regions, we found significant positive relationships between flea abundance and either the number of host species they exploited or the average taxonomic distance among those host species. This was true whether we used mean flea abundance or the maximum abundance they achieved on their optimal host. Although fleas tended to exploit more host species in regions with either larger number of available hosts or more taxonomically diverse host faunas, differences in host faunas between regions had no clear effect on the abundance–host specificity relationship. Overall, the results support the resource breadth hypothesis: fleas exploiting many host species or taxonomically unrelated hosts achieve higher abundance than specialist fleas. We conclude that generalist parasites achieve higher abundance because of a combination of resource availability and stability.