Gesture is one of the most ubiquitous forms of communication in the animal kingdom. However, little is known about the motor circuits that control such behavior. One possibility is that neural control of gesture might arise through repurposing and specializing ancestral circuits that control other forms of communication, which has been proposed to occur for circuits in some bird species through brain region or pathway duplications of an ancient motor learning pathway. We investigated the brain regions that control woodpecker drumming. We used a set of conserved molecular markers typically expressed in brain areas that control learned vocalizations in oscines. This approach identified two forebrain nuclei that exhibit striking neuroanatomical and molecular similarity to those found in the avian song system—the RA and LMAN, respectively. Both areas showed increased neural activity (immediate early gene) induced expression when birds drummed during territorial interactions, but not when they vocalize or move around during these interactions. Similar substrates also exist in the brains in two distantly related woodpecker species that also drum. Thus, we uncovered putative forebrain substrates associated with the production of an elaborate gestural display in the downy woodpecker, which may be shared across the woodpecker phylogeny. We suggest that ancestral forebrain circuits that control and refine motor patterns for communication, including those that gave rise to song control system in oscines, may be repurposed for drumming in woodpeckers. In both cases, communication may underlie the evolution of innovation, such as elaborate gestural displays that mediate aspects of socio-sexual behavior.