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Negative frequency-dependent selection (FDS), where rare genotypes are favoured by selection, is commonly invoked as a mechanism explaining the maintenance of genetic variation in plant defences. However, empirical tests of FDS in plant-herbivore interactions are lacking. We evaluated whether the oviposition preference of the specialist herbivore Lema daturaphila is a mechanism through which this herbivore can exert FDS on its host plant Datura stramonium. The frequency of contrasting resistance-tolerance strategies was manipulated within experimental plots, and the plants were exposed to a similar initial density of their natural herbivore. Herbivore oviposition preference and final density, as well as plant damage and seed production, were estimated. Overall, we found that the high-resistant-low-tolerant genotypes produced four times more seeds when common than when rare, whereas the high-tolerant-low-resistant genotypes achieved twice its fitness when rare than when common. This pattern was the result of differential oviposition preferences. In addition, when the high-resistant-low-tolerant genotypes were common, there was a three-fold decreased in herbivore final density which led to a decrease in damage level by 10%. Thus, in our experiment positive FDS seems to favour resistance over tolerance. We discuss how this result would change if the extent of herbivore local adaptation and damage modify the pattern of positive FDS acting on resistance and the optimal allocation to tolerance., (© 2015 European Society For Evolutionary Biology. Journal of Evolutionary Biology © 2015 European Society For Evolutionary Biology.)