Abstract Following unimanual training on a novel sequence of movements, sequence‐specific performance may improve overnight not only in the trained hand, but also in the hand afforded no actual physical experience. It is not clear, however, how transfer to the untrained hand is achieved. Here we examined whether and how interaction between the two primary motor cortices contributes to the performance of a sequence of movements, extensively trained a day before, by the untrained hand. To this end, we studied participants during the untrained‐hand performance of a finger‐to‐thumb opposition sequence (FOS), intensively trained a day earlier (T‐FOS), and a similarly constructed, but novel, untrained FOS (U‐FOS). Changes in neural signals driven by task performance were assessed using fMRI. To minimize potential differences due to the rate of sequence execution per se, participants performed both sequences at an identical paced rate. The analyses showed that the superior fluency in executing the T‐FOS, compared to the U‐FOS, was associated with higher activity within the primary motor cortex (M1), bilaterally, for the T‐FOS. The differential responses in the “trained” M1 were positively correlated with experience‐related differences in the functional connectivity between the “trained” M1 and (1) its left homolog, and (2) the left dorsal premotor cortex. However, no significant correlation was evident between the changes in connectivity in these two routes. These results suggest that the transfer of sequence‐specific information between the two primary motor cortices is predominantly mediated by excitatory mechanisms driven by the “trained” M1 through at least two independent neural pathways. This article is protected by copyright. All rights reserved