Cortical-basal ganglia circuits have a critical role in motor control and motor learning. In songbirds, the anterior forebrain pathway (AFP) is a basal ganglia-forebrain circuit required for song learning and adult vocal plasticity but not for production of learned song. Here, we investigate functional contributions of this circuit to the control of song, a complex, learned motor skill. We test the hypothesis that neural activity in the AFP of adult birds can direct moment-by-moment changes in the primary motor areas responsible for generating song. We show that song-triggered microstimulation in the output nucleus of the AFP induces acute and specific changes in learned parameters of song. Moreover, under both natural and experimental conditions, variability in the pattern of AFP activity is associated with variability in song structure. Finally, lesions of the output nucleus of the AFP prevent naturally occurring modulation of song variability. These findings demonstrate a previously unappreciated capacity of the AFP to direct real-time changes in song. More generally, they suggest that frontal cortical and basal ganglia areas may contribute to motor learning by biasing motor output towards desired targets or by introducing stochastic variability required for reinforcement learning.