The primate brain exhibits complex cellular and connectomic organization that remains elusive. Here, we present a three-dimensional multi-omic atlas of the marmoset brain, integrating single-cell spatial transcriptomics with multi-modal neuroimaging and connectomics. Our analysis reveals that cortical organization is shaped by opposing molecular gradients emanating from allocortical and primary sensory regions and converging in association cortices, reconciling competing hypotheses of cortical expansion. This gradient underlies gradual and abrupt transcriptomic transitions defining cortical boundaries and aligns with molecular architecture in the thalamus and striatum, reflecting coordinated cortico-subcortical interactions. The marmosetdefault mode-like network, positioned at the apex of gradient convergence, exhibits the most complex molecular identity, with the frontal pole sharing transcriptomic, but not connectomic, features of this network. Notably, cross-species analysis highlights shared molecular specializations in human and marmoset auditory cortices, suggesting convergent evolution for complex vocal communication. This integrative resource provides fundamental insights into primate cortical organization, specialization, and evolution.
