Systems consolidation is a process by which new experiences are initially encoded in the hippocampus and subsequently transferred to the cortex, facilitating integration into long-term memory networks. Our recent study showed that the precise temporal dynamics of cross-area coupling between prefrontal cortex (PFC) and primary motor cortex (M1) can demarcate the transition to cortical stabilization and task performance, reducing involvement of the hippocampus. Here, we demonstrate the causal role of precise coupling in PFC-M1 sleep slow oscillation (SO) for motor memory stabilization. Using a skill learning task, we monitored cross-area coupling during NREM sleep and changes in reach-to-grasp motor task performance. Optogenetic interventions were applied to manipulate PFC-M1 SO coupling. Interestingly, disturbances in PFC activity during PFC-M1 coupled SO in sleep led to delayed increases in PFC-M1 coordination and slower stabilization of motor task performance – suggesting the causal impact of PFC-M1 coupling on evolving cortical representations during systems consolidation. Notably, the slower increases in PFC-M1 SO coupling were associated with disruptions and delayed enhancements of cross-area coupling during spindle trains, occurring in temporal clusters. Specifically, our results indicate that PFC SO could serve as predictors of the occurrence of M1 spindle trains. These results provide evidence for the causal role of PFC-M1 dialogue in memory representations during long-term motor learning and adaptation.