Highly coevolved pollination mutualism accompanied by reciprocal diversification has been known in only two plant genera, Ficus (Moraceae) and Yucca (Agavaceae), which are pollinated exclusively by obligate seed-parasitic wasps and moths, respectively. An additional, highly diversified, species-specific pollination mutualism between a monoecious tree genus, Glochidion (Euphorbiaceae), and a moth genus, Epicephala (Gracillariidae), is presented here. At night, the small female moth actively deposits pollen on the cryptic stigma of the female flower by using its proboscis, then oviposits into the style. The moth larva infests only a portion of the developing seeds within fruit. We confirmed that at least three Glochidion species are pollinated only by their respective seed-parasitic moth species, which could be distinguished by genitalic morphology and mitochondrial DNA sequences. These results and widespread evidence of limited seed infestation by the moths associated with Glochidion species suggest that speciation based on the highly specialized Glochidion stylar structure and moth oviposition behavior have promoted species diversification in Glochidion and its pollinators.