In mammals, sleep states are associated with neuronal plasticity subserving learning and memory. In the zebra finch, neural activity throughout the “song system” is strongly modulated by sleep and wake states. Cells in the premotor robust nucleus of the arcopallium (RA), display spontaneous high frequency bursts during sleep, some of which recapitulate the highly stereotyped premotor burst patterns observed during singing. Premotor bursting patterns in adult RA are also particularly susceptible to modification across periods of sleep. In juvenile zebra finches, behavioral data have also demonstrated a sleep-dependent component of song learning during the sensitive period, but the underlying neural mechanisms of sleep in plastic changes in the song system are unknown. To investigate the hypothesis that sleep activity in the song system premotor pathway participates in song learning, we recorded the entire vocal ontogeny of individual birds, as well as more limited infrared video of sleep behavior, electroencephalograms and spiking activity of individual cells in RA in juveniles during nighttime sleep on multiple nights prior to and following the onset of tutor song exposure. Results from these experiments demonstrate that bursting activity in RA during nighttime sleep reflects information specific to the particular song model a bird is exposed to, is strongly influenced by auditory feedback during singing, and that RA bursting activity reflects the structure of the bird’s own vocalizations. As well, the first changes in RA sleep activity induced by tutor song exposure appear to precede the first changes in vocal output. These results support the hypothesis that the widely observed high frequency bursting activity during sleep in the song system premotor pathway plays an active role in song learning.