This first ultrastructural study of oogenesis in a placental viviparous onychophoran describes oocyte differentiation, cell interactions and reveals various unusual cellular features. The viviparous onychophoran Plicatoperipatus jamaicensis has paired ovaries medially located, attached to the dorsal body wall by muscular terminal filaments. The rest of the female reproductive tract consists of paired spermathecae oviduct/uteri (hereafter referred to as uterus). Bulbous spermathecae are joined to the oviducts by ducts. Also continuous with the oviduct lumen are two tubular structures whose lumina open to the hemolymph. The uteri contain a progression of developmental stages from implantation through stalked morulae, blastocysts, larvae and juveniles about to be born. Growing oocytes are characterized by large germinal vesicles showing synaptonemal complexes. Oocytes are surrounded by flattened follicle cells that possess extensive bundles of thick and thin filaments. Mature oocytes contain little or no yolk, but are unique among organisms in accumulating a large central reservoir of stored glycogen. The lack of yolk reflects the placental viviparous nature of the reproductive process. The glycogen reservoir provides a rapidly accessible energy source for early developmental stages. Particularly prominent also are unusually extensive and highly elaborate Golgi complexes in the cortical and peri-nuclear ooplasm. While extensive Golgi complexes have been described in oocytes of a variety of species, the particularly exaggerated size and amount of Golgi in these onychophorans suggests they may provide excellent material for the study of Golgi function. The features of the oocyte and placental viviparity show this is an ideal model to investigate the nature of the placental reproductive process analogous to mammals in an invertebrate and its implications to oogenesis.