Abstract: The vestibulo‐ocular reflex (VOR) stabilizes the visual image on the retina during head movement by counter‐rotating the eyes in the head. The VOR is under adaptive control and has been extensively used to investigate sensorimotor transformations and motor learning. The cerebellar flocculus (FL) is intimately involved in VOR motor control and learning, because its sole output, the Purkinje cell firing pattern, modulates during visual‐vestibular interaction paradigms that induce motor learning, and flocculectomy impairs the ability to modify the VOR. However, the role of the FL in VOR motor learning and the possibility of another neuronal site responsible for learning have been controversial. Currently, we performed single unit recordings of FL Purkinje cells during adaptation of the vertical (V) VOR in squirrel monkeys and used a system identification approach to localize the adaptable neuronal sites responsible for VVOR motor learning. We demonstrated that there are multiple adaptive sites: one upstream or in the FL, another in the non‐FL pathway; change in the former site is in the wrong direction to cause the observed VVOR gain change, whereas that in the latter site is in the correct direction. The possibility that FL Purkinje cells convey an error signal to their target neurons that can be used to aid learning is discussed.