Previous studies have demonstrated that imitating a face can be relatively automatic and reflexive. In contrast, opposing facial expressions may require engaging flexible, cognitive control. However, few studies have examined the degree to which imitation and opposition of facial movements recruit overlapping and distinct neural regions. Furthermore, little work has examined whether opposition and imitation of facial movements differ between emotional and averted eye gaze facial expressions. This study utilized a novel task with 40 participants to compare passive viewing, imitation and opposition of emotional faces looking forward and neutral faces with averted eye gaze [(3: Look, Imitate, Oppose) x (2: Emotion, Averted Eye)]. Imitation and opposition of both types of facial movements elicited overlapping activation in frontal, premotor, superior temporal and anterior intraparietal regions. These regions are recruited during cognitive control, face processing and mirroring tasks. For both emotional and averted eye gaze photos, opposition engaged the superior frontal gyrus, superior temporal sulcus and the anterior intraparietal sulcus to a greater extent compared to imitation. Finally, stimulus type and instruction interacted, such that for the eye gaze condition only, greater activation was observed in the dorsal anterior cingulate (dACC) during opposition compared to imitation, while no significant dACC differences were observed for the emotional expression conditions, which instead showed significantly greater activation in the middle and frontal pole. Overall these results showed significant overlap between imitation and opposition, as well as increased activation of these regions to generate an opposing facial movement relative to imitating.