Parasitoid wasps of the subfamily Telenominae (Hymenoptera: Platygastroidea, Platygastridae) develop as immatures within the eggs of other insects (Lepidoptera, Hemiptera, Diptera and Neuroptera). Rearing records indicate that individual species are restricted to attack hosts within only one of these four main groups. We conducted a phylogenetic analysis of the group using sequence data from multiple genes (18S, 28S, COI, EF-1α) to assess the pattern of shifts among host groups and to test the monophyly of and relationships among genera and species-groups. Telenominae sensu Masner—that is, including only the nominate tribe Telenomini—is not monophyletic. Representatives of the Psix group of genera (Psix Kozlov & Lê and Paratelenomus Dodd) form a monophyletic group that is sister to Gryon Haliday (Scelioninae: Gryonini) and are excluded from the subfamily. The remaining telenomines are monophyletic. The genus Phanuromyia Dodd and the crassiclava group of Telenomus Haliday, both recorded as parasitoids of planthopper eggs (Hemiptera: Auchenorrhyncha, Fulgoroidea), form a monophyletic group that is sister to all other telenomines exclusive of the Psix group. Twenty-nine species of the crassiclava and aradi groups of Telenomus are transferred to Phanuromyia as new combinations. Basal elements of the remaining species are all in groups reared from the eggs of true bugs (Heteroptera), primarily the stink bugs (Pentatomoidea) and seed bugs (Lygaeoidea). A shift to parasitism of lepidopteran eggs evolved within a single clade, occurring either one or two times. From this clade a small group of species, the Telenomus tabanivorus group, subsequently shifted to parasitism of egg masses of true flies (Tabanidae and Stratiomyiidae). Aholcus Kieffer and Platytelenomus Dodd both belong to the clade of lepidopteran parasitoids and are considered as junior synonyms of Telenomus (new synonymy for Aholcus). The monophyletic status of the two core genera, Telenomus and Trissolcus could not be resolved using these data. The phylogenetic pattern of host shifts suggests comparisons among taxa that may be fruitful in elucidating mechanisms by which parasitoids locate their hosts, the proximate factors that determine the host range, and the changes in these factors that influence host changes.