Bridging between brain activity and machine control, brain-computer interface (BCI) can be employed to activate distributed neural circuits implicated in a specific aspect of motor control. Using a motor imagery-based BCI paradigm, we previously found a disinhibition within the primary motor cortex contralateral to the imagined movement, as evidenced by event-related desynchronization (ERD) of oscillatory cortical activity. Yet it is unclear whether this BCI approach does selectively facilitate corticomotor representations targeted by the imagery. To address this question, we used brain state-dependent transcranial magnetic stimulation while participants performed kinesthetic motor imagery of wrist movements with their right hand and received online visual feedback of the ERD. Single and paired-pulse magnetic stimulation were given to the left primary motor cortex at a low or high level of ERD to assess intracortical excitability. While intracortical facilitation showed no modulation by ERD, short-latency intracortical inhibition was reduced the higher the ERD. Intracortical disinhibition was only found in the agonist muscle targeted by motor imagery at high ERD level, but not in the antagonist muscle. Single pulse motor-evoked potential was also increased the higher the ERD. However, at high ERD level, this facilitatory effect on overall corticospinal excitability was not selective to the agonist muscle. Analogous results were found in two independent experiments, in which participants either performed kinesthetic motor imagery of wrist extension or flexion. Our results showed that motor imagery-based BCI can selectively disinhibit the corticomotor output to the agonist muscle, enabling effector-specific training in patients with motor paralysis.