The six known Costa Rican species of the cainpoplegine ichneumonid genus Cryplophion Viereck are described and keyed. The distribution of species throughout Costa Rica is detailed based on data gathered by an intensive Malaise trap survey of the ichneumonids of the country. Five new species are recognized: C. espinorai, C.guillermoi, C. manueli, C. moragai and C. tickelli, and a sixth, C. inaequalipes (Cresson) redescribed. The monophyly of the genus is demonstrated and the phylogeny of the Costa Rican species reconstructed. Host relationships have been established for all species in Costa Rica; they develop as koinobiont endoparasitoids of first to third instar larvae of Sphingidae or Saturniidae. Analysis of the host relationships from a phylogenetic perspective suggested that the genus first evolved using macroglossine sphingid larvae feeding on rubiaceous understorey plants as hosts, and subsequently diversified to utilize sphingine sphingids and ceratocampine saturniids feeding on a variety of food-plants. Most species appear to be monophagous and oligophagy is apparently a derived feature of one sister-species pair, C. espinozai and C. manueli. In Santa Rosa National Park, Costa Rica, only a small proportion of the species of Saturniidae and Sphingidae present are used as hosts by Cyptophion species. No one host species is parasitized by more than one Cryptophion species. No species of Cryptophion is known to parasitize more than one host species feeding on any one plant species. The monophagous species C. inaequalipes is only known to develop in its sphingid host when that host is feeding on one of its two alternative food-plants.