The mammalian cortex is a laminar structure composed of many areas and cell types densely interconnected in complex ways, for which generalizable principles of organization remain mostly unknown. Here, we present a significant expansion of the Allen Mouse Brain Connectivity Atlas resource 1 , with ~1,000 new tracer experiments in cortex and its major satellite structure, the thalamus, using Cre driver lines to comprehensively and selectively label brain-wide connections by layer and projection neuron class. We derived a set of generalized anatomical rules describing corticocortical, thalamocortical and corticothalamic projections through observations of axon termination patterns. We built a model to assign connection patterns between areas as either feedforward or feedback, and generated testable predictions of hierarchical positions for individual cortical and thalamic areas and for cortical network modules. Our results reveal cell class-specific connections are organized in a shallow hierarchy within the mouse cortical thalamic network.