Modular organization, the division of the cerebral cortex into functionally distinct subregions, is well established in the primate sensorimotor cortex, but debated in the cognitive association cortex, including the lateral prefrontal cortex (PFC). So far, single-unit recordings have not confirmed the prefrontal rostro-caudal gradients observed in neuroimaging and neuroanatomical experiments. To bridge these microscale and macroscale perspectives, we obtained microelectrode recordings with exceptional spatial coverage from the PFC of monkeys engaged in a working memory task. Neighboring electrodes shared task-related neural dynamics that were stable across recording sessions and formed spatially continuous, mesoscale clusters with distinct local and long-range fronto-parietal connectivity. Spiking activity was cluster-specific and related to either the encoding, maintenance or decoding of working memory content. Our findings support parcellation of the PFC by cognitive control operations rather than by processed information, indicating that modularity is a fundamental architectural principle across the primate cortex.