Variations in cortical oscillations in the alpha (7-14 Hz) and beta (15-29 Hz) range have been correlated with attention, working memory, and stimulus detection. The mu rhythm recorded with magnetoencephalography (MEG) is a prominent oscillation generated by Rolandic cortex containing alpha and beta bands. Despite its prominence, the neural mechanisms regulating mu are unknown. We characterized the ongoing MEG mu rhythm from a localized source in the finger representation of primary somatosensory (SI) cortex. Subjects showed variation in the relative expression of mu-alpha or mu-beta, which were nonoverlapping for roughly 50% of their respective durations on single trials. To delineate the origins of this rhythm, a biophysically principled computational neural model of SI was developed, with distinct laminae, inhibitory and excitatory neurons, and feedforward (FF, representative of lemniscal thalamic drive) and feedback (FB, representative of higher-order cortical drive or input from nonlemniscal thalamic nuclei) inputs defined by the laminar location of their postsynaptic effects. The mu-alpha component was accurately modeled by rhythmic FF input at approximately 10-Hz. The mu-beta component was accurately modeled by the addition of approximately 10-Hz FB input that was nearly synchronous with the FF input. The relative dominance of these two frequencies depended on the delay between FF and FB drives, their relative input strengths, and stochastic changes in these variables. The model also reproduced key features of the impact of high prestimulus mu power on peaks in SI-evoked activity. For stimuli presented during high mu power, the model predicted enhancement in an initial evoked peak and decreased subsequent deflections. In agreement, the MEG-evoked responses showed an enhanced initial peak and a trend to smaller subsequent peaks. These data provide new information on the dynamics of the mu rhythm in humans and the model provides a novel mechanistic interpretation of this rhythm and its functional significance.