New World leaf-nosed bats (Phyllostomidae) occupy an enormous range of dietary niches and natural selection has shaped an array of morphological and sensory adaptations to exploit these dietary niches. However, the molecular mechanisms that allowed populations to depart from their ancestral insectivorous diet and detect novel resources, such as nectar or fruit, are unknown. Phyllostomids need to find these resources while flying in the dark, and behavioral evidence has shown the sense of smell is a critical supplement to echolocation for detecting food in a cluttered environment. We hypothesised that the genetic machinery governing the detection of plant volatiles to also be shaped by natural selection. To test this, we sequenced the transcriptomes of the main olfactory epithelium and identified the olfactory receptor profiles in over 20 phyllostomids with divergent diets. We identified many duplication events unique to particular bat subfamilies with unique diets. Some of these duplications occurred within groups with increased rates of speciation, and may be related to their diversification. For example, a unique cluster of olfactory receptors in subfamily OR2/13 is present only in fig-eating phyllostomids (Stenodermatinae). Stenodermatines have a significantly higher speciation rate compared to all other bats, attributed to their ability to exploit the novel dietary niche of consuming hard-fruits. This duplication of receptors that occurred prior to the divergence of stenodermatines may be connected to the diversity of olfactory receptor ligand profiles the ancestral stenodermatines explored. Our study illuminates how the olfactory receptor evolution may have opened up novel dietary niches for bats.