Two major mechanisms of aesthetic evolution have been suggested. One focuses on naturally selected preferences (Evolutionary Aesthetics), while the other describes a process of evaluative coevolution whereby preferences coevolve with signals. Signaling theory suggests that expertise moderates these mechanisms. In this article we set out to verify this hypothesis in the domain of art and use it to elucidate Western modern art's deviation from naturally selected preferences. We argue that this deviation is consistent with a Coevolutionary Aesthetics mechanism driven by prestige-biased social learning among art experts. In order to test this hypothesis, we conducted two studies in which we assessed the effects on lay and expert appreciation of both the biological relevance of the given artwork's depicted content, viz., facial beauty, and the prestige specific to the artwork's associated context (MoMA). We found that laypeople appreciate artworks based on their depictions of facial beauty, mediated by aesthetic pleasure, which is consistent with previous studies. In contrast, experts appreciate the artworks based on the prestige of the associated context, mediated by admiration for the artist. Moreover, experts appreciate artworks depicting neutral faces to a greater degree than artworks depicting attractive faces. These findings thus corroborate our contention that expertise moderates the Evolutionary and Coevolutionary Aesthetics mechanisms in the art domain. Furthermore, our findings provide initial support for our proposal that prestige-driven coevolution with expert evaluations plays a decisive role in modern art's deviation from naturally selected preferences. After discussing the limitations of our research as well as the relation that our results bear on cultural evolution theory, we provide a number of suggestions for further research into the potential functions of expert appreciation that deviates from naturally selected preferences, on the one hand, and expertise as a moderator of these mechanisms in other cultural domains, on the other.