Abstract The alpha rhythm is the longest studied brain oscillation and has been theorized to play a key role in cognition. Still, its physiology is poorly understood. In this study, we used micro and macro electrodes in surgical epilepsy patients to measure the intracortical and thalamic generators of the alpha rhythm during quiet wakefulness. We first found that alpha in posterior cortex propagates from higher-order anterosuperior areas towards the occipital pole, consistent with alpha effecting top-down processing. This cortical alpha leads pulvinar alpha, complicating prevailing theories of a thalamic pacemaker. Finally, alpha is dominated by currents and firing in supragranular cortical layers. Together, these results suggest that the alpharhythm likely reflects short-range supragranular feedback which propagates from higher to lower-order cortex and cortex to thalamus. These physiological insights suggest how alpha could mediate feedback throughout the thalamocortical system.