The human visual system can be divided into over two-dozen distinct areas, each of which contains a topographic map of the visual field. A fundamental question in vision neuroscience is how the visual system integrates information from the environment across different areas. Using neuroimaging, we investigated the spatial pattern of correlated BOLD signal across eight visual areas on data collected during rest conditions and during naturalistic movie viewing. The correlation pattern between areas reflected the underlying receptive field organization with higher correlations between cortical sites containing overlapping representations of visual space. In addition, the correlation pattern reflected the underlying widespread eccentricity organization of visual cortex, in which the highest correlations were observed for cortical sites with iso-eccentricity representations including regions with non-overlapping representations of visual space. This eccentricity-based correlation pattern appears to be part of an intrinsic functional architecture that supports the integration of information across functionally specialized visual areas.