An adult olivocerebellar axon ramifies into about seven climbing fibers that innervate single Purkinje cells arranged in a longitudinal microzone. To clarify the developmental basis of this projection, individual olivocerebellar axons were labeled with biotinylated dextran amine injected into the inferior olive in rats at postnatal days 4–7. The entire trajectories of single olivocerebellar axons and single terminal arbors of climbing fibers were reconstructed from serial sections of the cerebellum and medulla. Single axons ramified into climbing fibers that terminated in a narrow band-shaped area comparable to the adult microzone. This indicated that olivocerebellar microzones are predetermined. Terminal arbors of climbing fibers were remodeled from loose creeper type, through intermediate transitional type, into dense nest type. Each olivocerebellar axon had some 100 nascent climbing fibers in the creeper stage, whereas each axon had about 10 climbing fibers and about as many atrophic climbing fibers in the nest stage. This decrease indicated that overabundant nascent climbing fibers degenerate concomitantly with the remodeling of remaining climbing fibers. Atrophic terminal arbors and non-climbing fiber thin collaterals were considered the intermediate forms of degenerating climbing fibers. This remodeling and degeneration of climbing fibers may be related to the electrophysiological regression of climbing fiber-Purkinje cell synapses. The remodeling of climbing fibers occurred earliest in lobules VIII (caudal part) and IXa-b, and then in lobules IXc and X. The more developed granular layer in these areas compared to other areas suggests that the cortical environment triggers climbing fiber remodeling. J. Comp. Neurol. 487:93–106, 2005. © 2005 Wiley-Liss, Inc.