Neurofeedback (NF) training based on motor imagery is increasingly used in neurorehabilitation with the aim to improve motor functions. However, the neuroplastic changes underpinning these improvements are poorly understood. Here, we used mental finger individuation, i.e., the selective facilitation of single finger representations without producing overt movements, as a model to study neuroplasticity induced by NF. To enhance mental finger individuation, we used transcranial magnetic stimulation (TMS)-based NF training. During motor imagery of individual finger movements, healthy participants were provided visual feedback on the size of motor evoked potentials, reflecting their finger-specific corticospinal excitability. We found that TMS-NF improved the top-down activation of finger-specific representations. First, intracortical inhibitory circuits in the primary motor cortex were tuned after training such that inhibition was selectively reduced for the finger that was mentally activated. Second, motor imagery finger representations in sensorimotor areas assessed with functional MRI became more distinct after training. Together, our results indicate that the neural underpinnings of finger individuation, a well-known model system for neuroplasticity, can be modified using TMS-NF guided motor imagery training. These findings demonstrate that TMS-NF induces neuroplasticity in the sensorimotor system, highlighting the promise of TMS-NF on the recovery of fine motor function.