The mechanisms of learning involved in brain self-regulation have still to be unveiled to exploit the full potential of this methodology for therapeutic interventions. This skill of volitionally changing brain activity presumably resembles motor skill learning which in turn is accompanied by plastic changes modulating resting state networks. Along these lines, we hypothesized that brain regulation and neurofeedback would similarly modify intrinsic networks at rest while presenting a distinct spatio-temporal pattern. High-resolution electroencephalography preceded and followed a single neurofeedback training intervention of modulating circumscribed sensorimotor low β-activity by kinesthetic motor imagery in eleven healthy participants. The participants were kept in the deliberative phase of skill acquisition with high demands for learning self-regulation through stepwise increases of task difficulty. By applying the corrected imaginary part of the coherency function, we observed increased functional connectivity of both the primary motor and the primary somatosensory cortex with their respective contralateral homologous cortices in the low β-frequency band which was self-regulated during feedback. At the same time, the primary motor cortex—but none of the surrounding cortical areas—showed connectivity to contralateral supplementary motor and dorsal premotor areas in the high β-band. Simultaneously, the neurofeedback target displayed a specific increase of functional connectivity with an ipsilateral fronto-parietal network in the α-band while presenting a de-coupling with contralateral primary and secondary sensorimotor areas in the very same frequency band. Brain self-regulation modifies resting state connections spatially selective to the neurofeedback target of the dominant hemisphere. These are anatomically distinct with regard to the cortico-cortical connectivity pattern and are functionally specific with regard to the time domain of coherent activity consistent with a Hebbian-like sharpening concept.