Specific regions in the cognitive cerebellum are connected to distinct cerebral association networks. Do these cerebellar regions exhibit functional specialization similar to the cerebral cortex? Here, we mapped the cerebellum within intensively studied participants (N = 15) first using connectivity to estimate regions linked to specific networks and then prospectively testing functional response properties in task data within each individual's own idiosyncratic anatomy. A large megacluster extending across Crus I/II was consistently found with subregions linked to five higher-order association networks. A more variable smaller association cluster was found in lobule IX. Within the Crus I/II megacluster, specific cerebellar regions responded to domain-flexible cognitive control, while juxtaposed regions differentially responded to language, social, and spatial/episodic task demands. Similarly organized clusters also exist in the caudate consistent with the presence of multiple basal ganglia-cerebellar-cerebral cortical circuits that maintain functional specialization across their entire distributed extents.