The evolution of vocal communication in humans required the emergence of not only voluntary control of the vocal apparatus and a flexible vocal repertoire, but the capacity for vocal learning. All of these capacities are lacking in non-human primates, suggesting that the vocal brain underwent significant modifications during human evolution. We review research spanning from early neurophysiological descriptions of great apes to the state of the art in human neuroimaging on the neural organization of the larynx motor cortex, the major regulator of vocalization for both speech and song in humans. We describe changes to the location, structure, function, and connectivity of the larynx motor cortex in humans compared with non-human primates, including critical gaps in the current understanding of the brain systems mediating vocal control and vocal learning. We explore a number of models of the origins of the vocal brain that incorporate findings from comparative neuroscience, and conclude by presenting a summary of contemporary hypotheses that can guide future research.