Animals that exploit living spaces of other animals (inquilines) may have specialized traits that adapt them to extended phenotypes of their ‘hosts’. These adaptations to host traits may incur fitness trade-offs that restrict the host range of an inquiline such that shifts to new hosts might trigger inquiline diversification. Speciation via host shifting has been studied in many animal parasites, but we know less about the role of host shifts in inquiline speciation. Synergus Hartig (Hymenoptera: Cynipidae: Synergini) is a speciose but taxonomically challenging genus of inquilines that feed inside galls induced by oak gall wasps (Hymenoptera: Cynipidae: Cynipini). Here, we report on a large collection of Synergus reared from galls of 33 oak gall wasp species in the upper Midwestern United States. We integrated DNA barcodes, morphology, ecology, and phenology to delimit putative species of Synergus and describe their host ranges. We find evidence of at least 23 Synergus species associated with the 33 gall wasp hosts. At least five previously described Synergus species are each complexes of two to five species, while three species fit no prior description. We find evidence that oak tree phylogeny and host gall morphology define axes of specialization for Synergus. The North American Synergus have experienced several transitions among gall hosts and tree habitats and their host use is correlated with reproductive isolation. It remains too early to tell whether shifts to new hosts initiate speciation events in Synergus inquilines of oak gall wasps, or if host shifts occur after reproductive isolation has already evolved.