For primates, expressions of fear are thought to be powerful social signals. In laboratory settings, faces with fearful expressions have reliably evoked valence effects in inferior temporal cortex. However, because macaques use so called “fear grins” in a variety of different contexts, the deeper question is whether the macaque inferior temporal cortex is tuned to the prototypical fear grin, or to conspecifics signaling fear? In this study, we combined neuroimaging with the results of a behavioral task to investigate how macaques encode a wide variety of fearful facial expressions. In Experiment 1, we identified two sets of macaque face stimuli using different approaches; we selected faces based on the emotional context (i.e., calm vs. fearful), and we selected faces based on the engagement of action units (i.e., neutral vs. fear grins). We also included human faces in Experiment 1. Then, using fMRI, we found that the faces selected based on context elicited a larger valence effect in the inferior temporal cortex than faces selected based on visual appearance. Furthermore, human facial expressions only elicited weak valence effects. These observations were further supported by the results of a two-alternative, forced-choice task (Experiment 2), suggesting that fear grins vary in their perceived pleasantness. Collectively, these findings indicate that the macaque inferior temporal cortex is more involved in social intelligence than commonly assumed, encoding emergent properties in naturalistic face stimuli that transcend basic visual features. These results demand a rethinking of theories surrounding the function and operationalization of primate inferior temporal cortex.