How the human brain integrates internally-(i.e., mnemonic) and externally-oriented (i.e., perceptual) information is a long-standing puzzle in neuroscience. In particular, the internally-oriented networks like the default network (DN) and externally-oriented dorsal attention networks (dATNs) are thought to be globally competitive, which implies DN disengagement during cognitive states that drive the dATNs and vice versa. If these networks are globally opposed, how is internal and external information integrated across these networks? Here, using precision neuroimaging methods, we show that these internal/external networks are not as dissociated as traditionally thought. Using densely sampled high-resolution fMRI data, we defined individualized whole-brain networks from participants at rest, and the retinotopic preferences of individual voxels within these networks during an independent visual mapping task. We show that while the overall network activity between the DN and dATN is opponent at rest, a latent retinotopic code structures this global opponency. Specifically, the anti-correlation (i.e., global opponency) between the DN and dATN at rest is structured at the voxel-level by each voxel's retinotopic preferences, such that the spontaneous activity of voxels preferring similar visual field locations are more anti-correlated than those that prefer different visual field locations. Further, this retinotopic scaffold integrates with the domain-specific preferences of subregions within these networks, enabling efficient, parallel processing of retinotopic and domain-specific information. Thus, DN and dATN dynamics are opponent, but not competitive: voxel-scale anti-correlation between these networks preserves and encodes information in the negative BOLD responses, even in the absence of visual input or task demands. These findings suggest that retinotopic coding may serve as a fundamental organizing principle for brain-wide communication, providing a new framework for understanding how the brain balances and integrates internal cognition with external perception.