1. We assessed the host‐related niche breadth for D. koepferae and D. buzzatii, a pair of sibling cactophilic species with contrasting backgrounds of host use. We tested for the ‘Jack of all trades‐ Master of none’ scenario predicting a more evident exhibition in D. buzzatii rather than in the supposedly specialist D. koepferae.2. Additionally, using laboratory strains of both species selected for tolerance to extremely high concentrations of a columnar cacti's secondary metabolites, we tested whether adaptation to a high‐demanding host involved the loss of performance capabilities in other hosts.3. D. buzzatii was more affected by the artificial host shifts than D. koepferae which presented an overall better performance when rearing in novel columnar hosts.4. Artificially selected strains of D. buzzatii performed poorer in both novel and native natural hosts compared with control strain indicating that adaptation carried associated costs regarding the potential to exploit other cacti. Conversely, artificial evolution of the D. koepferae's strains did not translate into decreased performance in other hosts.5. D. buzzatii complied better with the predictions of the Jack of all trades‐Master of none hypothesis.6. Host specialization is a dynamic feature in the repleta group and a major driver of diversification in its evolutionary history. As the group presents an Opuntia breeder as the ancestral condition, D. buzzatii would represent not only a plesiomorphic state of host use but also the ancestral ecological strategy of specialization.