Learning involves a transformation of brain-wide operation dynamics. However, our understanding of learning-related changes in macroscopic dynamics is limited. Here, we monitored cortex-wide activity of the mouse brain using wide-field calcium imaging while the mouse learned a motor task over weeks. Over learning, the sequential activity across cortical modules became temporally more compressed, and its trial-by-trial variability decreased. Moreover, a new flow of activity emerged during learning, originating from premotor cortex (M2), and M2 became predictive of the activity of many other modules. Inactivation experiments showed that M2 is critical for the post-learning dynamics in the cortex-wide activity. Furthermore, two-photon calcium imaging revealed that M2 ensemble activity also showed earlier activity onset and reduced variability with learning, which was accompanied by changes in the activity-movement relationship. These results reveal newly emergent properties of macroscopic cortical dynamics during motor learning and highlight the importance of M2 in controlling learned movements. •Longitudinal wide-field calcium imaging of cortex during motor learning•Motor learning compressed and stabilized sequential activity across cortex•Motor learning altered the information flow across cortex•Premotor cortex acquired a leading role with motor learning With longitudinal wide-field calcium imaging, Makino et al. uncover novel principles underlying transformations of learning-related macroscopic dynamics, where motor learning leads to temporally compressed and more reliable sequential activation of cortical modules, with premotor cortex orchestrating the cortical activity.