Examining recent regulatory changes that drove human-specific traits is critical to understanding human adaptation. Here, we use dozens of ancient and present-day DNA methylation maps to identify regions where regulation changed in recent human evolution. We show that genes affecting the voice and face went through particularly extensive changes. This is evident both in the number of differentially methylated genes, and in the magnitude of alterations within each gene. We identify expansive changes in a network of genes regulating early skeletal development (SOX9, ACAN and COL2A1), and in NFIX, which controls facial projection and voice box (larynx) development. We propose that these regulatory changes played a key role in the shaping of the human face, as well as in the formation of the unique 1:1 configuration of the human vocal tract that is optimal for speech. Our results provide insight into the molecular mechanisms that formed the modern human face and vocal tract, and suggest that they arose after the split from the Neanderthal and the Denisovan.