Stroke-induced disturbances of large-scale cortical networks are known to be associated with the extent of motor deficits. We argue that identifying brain networks representative of motor behavior in the resting brain would provide significant insights for current neurorehabilitation approaches. Particularly, we aim to investigate the global configuration of brain rhythms and their relation to motor skill, instead of learning performance as broadly studied. We empirically approach this problem by conducting a three-dimensional physical space visuomotor learning experiment during electroencephalographic (EEG) data recordings with thirty-seven healthy participants. We demonstrate that across-subjects variations in average movement smoothness as the quantified measure of subjects' motor skills can be predicted from the global configuration of resting-state EEG alpha-rhythms (8-14 Hz) recorded prior to the experiment. Importantly, this neural signature of motor skill was found to be orthogonal to (independent of) task-as well as to learning-related changes in alpha-rhythms, which we interpret as an organizing principle of the brain. We argue that disturbances of such configurations in the brain may contribute to motor deficits in stroke, and that reconfiguring stroke patients' brain rhythms by neurofeedback may enhance post-stroke neurorehabilitation.