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Abstract Understanding the often antagonistic plant–herbivore interactions and how host defenses can influence herbivore dietary breadth is an area of ongoing study in ecology and evolutionary biology. Typically, host plants/fungi that produce highly noxious chemical defenses are only fed on by specialists. We know very little about generalist species that can feed and develop on a noxious host. One such example of generalists feeding on toxic host occurs in the mushroom‐feedingDrosophilafound in theimmigrans‐tripunctataradiation. Although these species are classified as generalists, their acceptable hosts include deadlyAmanitaspecies. In this study, we used behavioral assays to assess associations between one mushroom‐feeding species,Drosophila guttifera, and the deadlyAmanita phalloides. We conducted feeding assays to confirm the presence of cyclopeptide toxin tolerance. We then completed host preference assays in female flies and larvae and did not find a preference for toxic mushrooms in either. Finally, we assessed the effect of competition on oviposition preference. We found that the presence of a competitor's eggs on the preferred host was associated with the flies increasing the number of eggs laid on the toxic mushrooms. Our results highlight how access to a low competition host resource may help to maintain associations between a generalist species and a highly toxic host.