The functional topography of the human primary somatosensory cortex (S1) hand area is a widely studied model system to understand sensory organization and plasticity. It is so far unclear whether or not the underlying 3D structural architecture also shows a topographic organization. We used 7T MRI data to quantify layer-specific myelin, iron and mineralization in relation to population receptive field maps of individual finger representations. This 3D description allowed us to identify a characteristic profile of layer-specific myelin and iron deposition in the S1 hand area, but revealed an absence of structural differences between individual finger representations, and an absence of low-myelin borders between individual fingers. Both, however, were detected between the hand and the face areas. Using markers of responsivity, precision and sensorimotor integration, we additionally phenotyped these microstructural features with respect to their relation to BOLD signal change and behavior. We conclude that the 3D structural architecture of the human hand area is non-topographic, other than in some monkey species, which suggests a high degree of flexibility for functional finger organization and plasticity in humans.