The extent to which neural representations of fear experience depend on or generalize across the situational context has remained unclear. We systematically manipulated variation within and across three distinct fear-evocative situations including fear of heights, spiders, and social threats. Participants (n=21, 10 females and 11 males) viewed ∼20 second clips depicting spiders, heights, or social encounters, and rated fear after each video. Searchlight multivoxel pattern analysis (MVPA) was used to identify whether and which brain regions carry information that predicts fear experience, and the degree to which the fear-predictive neural codes in these areas depend upon or generalize across the situations. The overwhelming majority of brain regions carrying information about fear did so in a situation dependent manner. These findings suggest that local neural representations of fear experience are unlikely to involve a singular pattern, but rather a collection of multiple heterogeneous brain states.Significance Statement Much of the debate on the nature of emotion concerns the uniformity or heterogeneity of representation for particular emotion categories. Here we provide evidence that widely distributed activation patterns characteristic of recent neural signatures of fear reflect an amalgam of functionally heterogeneous brain states. Participants completed a novel fMRI task that parametrically examined subjective fear within and across three content-rich and naturalistic situations: fear of heights, spiders, and social threats. Using searchlight analysis and machine learning methods, we show that the overwhelming majority of brain regions that predict fear only do so for certain situations. These findings carry implications for the generalization of findings on fear across species, translational models of fear and anxiety, and developing neural signatures of fear.