The perception of facial expression and gaze-direction are important aspects of non-verbal communication. Expressions communicate the internal emotional state of others while gaze-direction offers clues to their attentional focus and future intentions. Cortical regions in the superior temporal sulcus (STS) play a central role in the perception of expression and gaze, but the extent to which the neural representations of these facial gestures are overlapping is unknown. In the current study 12 subjects observed neutral faces with direct-gaze, neutral faces with averted-gaze, or emotionally expressive faces with direct-gaze while we scanned their brains with functional magnetic resonance imaging (fMRI), allowing a comparison of the hemodynamic responses evoked by perception of expression and averted-gaze. The inferior occipital gyri, fusiform gyri, STS and inferior frontal gyrus were more strongly activated when subjects saw facial expressions than when they saw neutral faces. The right STS was more strongly activated by the perception of averted-gaze than direct-gaze faces. A comparison of the responses within right STS revealed that expression and averted-gaze activated distinct, though overlapping, regions of cortex. We propose that gaze-direction and expression are represented by dissociable overlapping neural systems.