Decades of human magnetic resonance imaging (MRI) research demonstrate that variance in neuroimaging phenotypes, including functional connectivity, relate to genetics1–5 and predict cognitive traits6–9. The functional connectome affords information transmission through the brain at various spatial scales, from global oscillations between broad cortical regions to fine-scale connections that underlie specific information processing10,11. In adults, while both the coarse- and fine-scale functional connectomes predict cognition6,12–14, the fine-scale connectome predicts twice as much cognitive variance15. Yet, past brain-wide association studies, particularly using large developmental samples, have limited their focus to the coarse connectome to understand the neural underpinnings of individual differences in cognition8,9,16–18. We studied resting-state fMRI in 1,115 children (including 389 twin pairs) and used functional alignment to afford access to individual differences in the fine-scale connectome10,19,20. We found that even though individual differences in the fine-scale connectome are more reliable than those in the coarse-scale connectome, they are less heritable. This surprising result indicates that genetically-determined versus experience-dependent factors in brain development have dissociable effects on these two spatial scales of the connectome. We show further that both connectome scales equally predict a more heritable trait (general cognitive ability) in childhood, but only the fine scale effectively predicts a more experience-driven trait (learning/memory). As such, the developing functional connectome resembles a LEGOⓇ set: the specific pieces a child has parameterizes what they will eventually build, but even when given identical sets, two children with unique experiences will build different creations.