Previous research has demonstrated learning in the pursuit system, but it is unclear whether these effects are the result of changes in visual or motor processing. The ability to maintain smooth pursuit during the transient disappearance of a visual target provides a way to assess pursuit properties in the absence of visual inputs. To study the long-term effects of learning on nonvisual signals for pursuit, we used an operant conditioning procedure. By providing a reinforcing auditory stimulus during periods of accurate tracking, we increased the pursuit velocity gain during target blanking from 0.59 in the baseline session to 0.89 after 8 to 10 daily sessions of training. Learning also reduced the occurrence of saccades. The learned effects generalized to untrained target velocities and persisted in the presence of a textured visual background. In a yoked-control group, the reinforcer was independent of the subjects' responses, and the velocity gain remained unchanged (from 0.6 to 0.63, respectively, before and after training). In a control group that received no reinforcer, gain increased slightly after repetition of the task (from 0.63 to 0.71, respectively, before and after training). Using a model of pursuit, we show that these effects of learning can be simulated by modifying the gain of an extra-retinal signal. Our results demonstrate that learned contingencies can increase eye velocity in the absence of visual signals and support the view that pursuit is regulated by extra-retinal signals that can undergo long-term plasticity.