Genetic factors have involved the gradual emergence of cortical areas since the neural tube begins to form, shaping the specialization of neural circuits in the human brain. Informed by invasive tract-tracing measurements, the cortex exhibits marked interareal variation in connectivity profiles, yet how this spatial variation is encoded in genetics remains unclear. Instead of considering a complex one-to-one mapping between genetic coding and interareal connectivity variation, we hypothesized the existence of a more efficient way that the organizing principles are embedded in genetic profiles to underpin the configuration of connectivity across the human cortex. Specifically, we found that a noninvasive neuroimaging measure, i.e., global connectopy derived from diffusion-weighted MRI tractography, reliably indexes the organizing principles of interareal connectivity variation, and it captures three dominant topographic patterns along the dorsoventral, rostrocaudal, and mediolateral axes of the cortex. We further found that the global connectopies converge to the gradients of vertex-by-vertex genetic correlation matrix on the phenotype of cortical morphology and the cortex-wide spatiomolecular gradients. Moreover, we found the critical role of genes related to brain morphogenesis in scaffolding the global connectopies. Our findings identify a common space linking genetic profilings and interareal connectivity variation, which may contribute to the accurate formation of cortical connections and arealization.