We studied the neural substrate of anticipation and learning of smooth pursuit eye movements in humans using fMRI. Both predictable and non-predictable eye movements, compared to baseline, activated a common network previously associated with oculomotor function. The temporal dynamics of activity in a subset of these areas suggested a strong correlation with type of condition. Specifically, differential decreases in activity were seen in dorsolateral prefrontal cortex and the intraparietal sulcus during the predictable condition. During the non-predictable condition the same areas exhibited evidence of high levels of activity that further increased throughout the condition. In contrast, differential increases associated with the predictable condition were seen in anterior cingulate and preSMA cortex regions. These changes in activity mirror the time course of the short-term learning of eye movements seen behaviourally, and are congruent with learning-related changes that have been reported for other motor paradigms.