A central component of wayfinding is the ability to maintain a consistent representation of one's facing direction (FD) when moving about the world. In rodents, head direction cells are believed to support this “neural compass,” but identifying a similar mechanism in humans during dynamic naturalistic navigation has been challenging. To address this issue, we acquired fMRI data from male and female human participants while they freely navigated through a virtual reality city. Encoding model analyses revealed voxel clusters in the posterior–medial cortex (the “retrosplenial complex”) and superior parietal lobule that exhibited reliable tuning as a function of FD. Crucially, these directional tunings were consistent across perceptually different versions of the city, spatially separated locations within the city, and motivationally distinct phases of the behavioral task. Analysis of the model weights indicated that these regions represent a broad range of possible FDs and that they do so by representing heading relative to the principal axis of the environment. These findings reveal specific mechanisms in the human brain that allow us to maintain a sense of direction during naturalistic, dynamic navigation.