The avian dorsal telencephalon has two vast territories, the nidopallium and the mesopallium, both of which have been shown to contribute substantially to higher cognitive functions. From their connections, these territories have been proposed as equivalent to mammalian neocortical layers 2 and 3, various neocortical association areas, or the amygdala, but whether these are analogies or homologies by descent is unknown. We investigated the molecular profiles of the mesopallium and the nidopallium with RNA-seq. Gene expression experiments established that the mesopallium, but not the nidopallium, shares a transcription factor network with the intratelencephalic class of neocortical neurons, which are found in neocortical layers 2, 3, 5, and 6. Experiments in alligators demonstrated that these neurons are also abundant in the crocodilian cortex and form a large mesopallium-like structure in the dorsal ventricular ridge. Together with previous work, these molecular findings indicate a homology by descent for neuronal cell types of the avian dorsal telencephalon with the major excitatory cell types of mammalian neocortical circuits: the layer 4 input neurons, the deep layer output neurons, and the multi-layer intratelencephalic association neurons. These data raise the interesting possibility that avian and primate lineages evolved higher cognitive abilities independently through parallel expansions of homologous cell populations.