The primary motor cortex (M1) is a central hub for motor learning and execution. M1 is composed of heterogeneous cell types, many exhibiting varying relationships to movement. Here, we employed an unbiased screen to tag active neurons at different stages of performance of a motor task. We characterized the relative cell type composition of active neurons across training and identified one cell type consistently enriched as training progressed: corticothalamic neurons (M1^CT). Using two-photon calcium imaging, we found that M1^CT activity is largely suppressed during movement, and this negative correlation with movement scales with movement vigor and augments with training. Closed-loop optogenetic manipulation of this population revealed that increasing M1^CT activity during forelimb movement significantly hinders execution, an effect that became stronger with training. Similar optogenetic manipulations, however, had little effect on locomotion. In contrast to M1^CT neurons, we observed that M1 corticospinal neurons positively correlate with movement, and that this positive correlation increases with learning. Finally, by examining the connectivity between M1^CT and corticospinal neurons, we uncovered that M1^CT neurons can suppress M1 corticospinal activity via feedforward inhibition, and that this inhibition scales with training. These results identify a novel permissive role of corticothalamic neurons in movement execution through suppression of inhibition of corticospinal neurons.