We studied host selection and exploitation, two crucial aspects of parasite ecology, in Achrysocharoides parasitoid wasps, which show remarkable host specificity and unusual offspring sex allocation. We estimated a molecular phylogeny of 15 Achrysocharoides species and compared this with host (plant and insect) phylogenies. This tri-trophic phylogenetic comparison provides no evidence for cospeciation, but parasitoids do show phylogenetic conservation of the use of plant genera. Patterns of sequence divergence also suggest that the parasitoids radiated more recently (or evolved much faster) than their insect hosts. Three main categories of brood production occur in parasitoids: (1) solitary offspring, (2) mixed sex broods and (3) separate (split) sex broods. Split sex broods are very rare and virtually restricted to Achrysocharoides, while the other types occur very widely. Our phylogeny suggests that split sex broods have evolved twice and provides evidence for a transition from solitary to mixed sex broods, via split sex broods, as predicted by theory.