Executing difficult actions with the left hand results in bilateral activity of motor areas along the precentral gyrus. Using TMS and fMRI, we explored the functional relationship between primary (M1) and premotor areas during unimanual actions, focusing on M1 activity in the ipsilateral hemisphere. Single-pulse TMS revealed that the amplitude of motor-evoked potentials (MEPs), elicited in the stationary right-hand muscles following left M1 stimulation, fluctuated with the state of homologous muscles in the moving left hand. This ipsilateral excitability was pronounced when the left-hand movements were more complex. We used fMRI to visualize the cortical dynamics during unimanual actions. Trial-by-trial fluctuations in ipsilateral M1 activity were correlated with contralateral M1 responses and this correlation increased with movement complexity. Consistent with previous studies, the left caudal precentral premotor area (pcPM) was engaged during movements of either hand. Following low-frequency rTMS over left pcPM, the correlation between the activity level in the two M1s increased. This finding indicates that left pcPM may regulate the unintentional mirroring of motor commands in M1 during unilateral movement.