Despite extensive research on inhibitory control (IC) and its neural systems, the questions of whether IC can be improved with training and how the associated neural systems change are understudied. Behavioral evidence suggests that performance on IC tasks improves with training but that these gains do not transfer to other tasks, and almost nothing is known about how activation in IC-related brain regions changes with training. Human participants were randomly assigned to receive IC training (N = 30) on an adaptive version of the stop-signal task (SST) or an active sham-training (N = 30) during 10 sessions across 3 weeks. Neural activation during the SST before and after training was assessed in both groups using functional magnetic resonance imaging. Performance on the SST improved significantly more in the training group than in the control group. The pattern of neuroimaging results was consistent with a proactive control model such that activity in key parts of the IC network shifted earlier in time within the trial, becoming associated with cues that anticipated the upcoming need for IC. Specifically, activity in the inferior frontal gyrus decreased during the implementation of control (i.e., stopping) and increased during cues that preceded the implementation of IC from pretraining to post-training. Also, steeper behavioral improvement in the training group correlated with activation increases during the cue phase and decreases during implementation in the dorsolateral prefrontal cortex. These results are the first to uncover the neural pathways for training-related improvements in IC and can explain previous null findings of IC training transfer.