The auditory cortex (AC) sends long-range projections to virtually all subcortical auditory structures. One of the largest and most complex of these—the projection between AC and inferior colliculus (IC; the corticocollicular pathway)—originates from layer 5 and deep layer 6. Though previous work has shown that these two corticocollicular projection systems have different physiological properties and network connectivities, their functional organization is poorly understood. Here, using a combination of traditional and viral tracers combined with in vivo imaging in both sexes of the mouse, we observed that layer 5 and layer 6 corticocollicular neurons differ in their areas of origin and termination patterns. Layer 5 corticocollicular neurons are concentrated in primary AC, while layer 6 corticocollicular neurons emanate from broad auditory and limbic areas in the temporal cortex. In addition, layer 5 sends dense projections of both small and large (>1 µm2 area) terminals to all regions of nonlemniscal IC, ...