The rodent somatosensory cortex includes well-defined examples of cortical columns—the barrel columns—that extend throughout the cortical depth and are defined by discrete clusters of neurons in layer 4 (L4) called barrels. Using the cell-type-specific Ntsr1-Cre mouse line, we found that L6 contains infrabarrels, readily identifiable units that align with the L4 barrels. Corticothalamic (CT) neurons and their local axons cluster within the infrabarrels, whereas corticocortical (CC) neurons are densest between infrabarrels. Optogenetic experiments showed that CC cells received robust input from somatosensory thalamic nuclei, whereas CT cells received much weaker thalamic inputs. We also found that CT neurons are intrinsically less excitable, revealing that both synaptic and intrinsic mechanisms contribute to the low firing rates of CT neurons often reported in vivo. In summary, infrabarrels are discrete cortical circuit modules containing two partially separated excitatory networks that link long-distance thalamic inputs with specific outputs. Layer 6 is a major input-output layer of neocortex, but key principles of its circuit organization are lacking. Crandall et al. reveal barrel-like structures called infrabarrels that include distinct excitatory circuits linking thalamic inputs with specific outputs, thus providing a framework for understanding the functional organization of layer 6.