The interactions between neocortical areas are fluid and state-dependent, but how individual neurons couple to cortex-wide network dynamics remains poorly understood. We correlated the spiking of neurons in primary visual (V1) and retrosplenial (RSP) cortex to activity across dorsal cortex, recorded simultaneously by widefield calcium imaging. Neurons were correlated with distinct and reproducible patterns of activity across the cortical surface; while some fired predominantly with their local area, others coupled to activity in distal areas. The extent of distal coupling was predicted by how strongly neurons correlated with the local network. Changes in brain state triggered by locomotion strengthened affiliations of V1 neurons with higher visual and motor areas, while strengthening distal affiliations of RSP neurons with sensory cortices. Thus, the diverse coupling of individual neurons to cortex-wide activity patterns is restructured by running in an area-specific manner, resulting in a shift in the mode of cortical processing during locomotion.