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Human brain structure topography is thought to be related in part to functional specialization. However, the extent of such relationships is unclear. Here, using a data-driven, multimodal approach for studying brain structure across the lifespan (N = 484, n = 260 females), we demonstrate that numerous structural networks, covering the entire brain, follow a functionally meaningful architecture. These gray matter networks (GMNs) emerge from the covariation of gray matter volume and cortical area at the population level. We further reveal fine-grained anatomical signatures of functional connectivity. For example, within the cerebellum, a structural separation emerges between lobules that are functionally connected to distinct, mainly sensorimotor, cognitive and limbic regions of the cerebral cortex and subcortex. Structural modes of variation also replicate the fine-grained functional architecture seen in eight well defined …