Although the inferior olivary nucleus of the opossum is small, sections stained either for Nissl substance, normal axons or cholinesterase activity reveal distinct medial, dorsal and principal nuclei. The medial nucleus contains three major subdivisions (labelled a, b, c after Bowman and Sladek, '73) and a group of neurons which is comparable to the cap of Kooy. In contrast to the cat and monkey, the major portion of the "medial" nucleus (subgroup a) lies lateral to the principal nucleus in rostral sections. The dorsal nucleus can also be subdivided, as can the principal nucleus which contains distinct dorsal and ventral lamellae. A small area is identified which based on position and connections may conform to the dorsal medial cell group. The experimental portion of the study provides evidence for an olivary projection from the motor-sensory cortex and a massive input from the midbrain (red nucleus, pretectum, midbrain tegmentum). In addition, the opossum inferior olive receives fibers from the deep cerebellar nuclei (cerebellar feedback loops), the spinal cord and the dorsal column nuclei. Of particular interest is the finding that fibers from the nucleus cuneatus and nucleus gracilis have distinctly different olivary targets and that those from the nucleus gracilis, but not the cuneate nucleus, overlap (in part, at least) with the direct spinal fibers. Other examples of overlapping fields of terminal degeneration are present and are discussed. In general our results reveal that although certain relationships between the nuclear divisions are different, the opossum olive conforms well to that of placental mammals and provides a basic mammalian model for future experimental electron microscopic and physiological studies.