The principles governing the functional organization and development of long-range network interactions in the neocortex remain poorly understood. Using in vivo widefield and two-photon calcium imaging of spontaneous activity patterns in mature ferret visual cortex, we find widespread modular correlation patterns that accurately predict the local structure of visually evoked orientation columns several millimeters away. Longitudinal imaging demonstrates that long-range spontaneous correlations are present early in cortical development before the elaboration of horizontal connections and predict mature network structure. Silencing feedforward drive through retinal or thalamic blockade does not eliminate early long-range correlated activity, suggesting a cortical origin. Circuit models containing only local, but heterogeneous, connections are sufficient to generate long-range correlated activity by confining activity patterns to a low-dimensional subspace via multisynaptic short-range interactions. These results suggest that local connections in early cortical circuits can generate structured long-range network correlations that guide the formation of visually evoked distributed functional networks.