Neurons that signal the direction and angular velocity of head movements (AHV cells) are critically important to process visual and spatial information. However, it has been challenging to isolate the sensory modality that drives them and to compre hensively map their cortical distribution. To address this, we developed a method that enables rotating awake, head-fixed mice under a two-photon microscope in a visual environment. Starting in layer 2/3 of the retrosplenial cortex, a key area for vision and navigation, we found that a significant fraction of rotation sensitive neurons report AHV. These tuning properties depend on vestibular input because they persist in darkness and are reduced when replaying visual flow to stationary animals. When mapping the spatial extent, we found AHV cells in all cortical areas that we explored, including motor, somatosensory, visual and posterior parietal cortex. Notably, the vestibular and visual contributions to AHV are area dependent. Thus, many cortical circuits have access to AHV, enabling a diverse integration with sensorimotor and cognitive information.