In the present study, Cryptosporidium oocysts were found, by light microscopy, in 37 fecal samples of peach-faced lovebirds (Agapornis roseicollis). Cryptosporidium avian genotype III was isolated in 13 of the 37 infected birds by sequence analysis of the small subunit ribosomal RNA and the actin genes. All of the birds showed chronic vomiting and weight loss with enlargement of isthmi, narrowed proventricular lumens, and thickened proventricular walls radiographically. Cryptosporidium parasites were found only in the ductal epithelium of the proventricular glands in three of the tissue samples provided for necropsy. To date, there have been no reports concerning the pathogenicity, nor the location, of avian genotype III in avian hosts. Our report confirms, for the first time, the presence of avian genotype III in peach-faced lovebirds in Japan and also reveals the location in the avian host.