While contemporary changes in feeding preferences have been documented in phytophagous insects, the mechanisms behind these processes remain to be fully clarified. In this context, the insect gut microbiome plays a central role in adaptation to novel host plants. The cucurbit frugivorous fruit fly Zeugodacus cucurbitae (Diptera, Tephritidae) has occasionally been reported on “unconventional” host plants from different families, including Solanaceae. In this study, we focus on wild parental (F₀) and semi-wild first filial (F₁) samples of Z. cucurbitae from multiple sites in La Réunion and explore how the gut microbiome composition changes when this fly is feeding on a non-cucurbit host (Solanum melongena). Our analyses show non-obvious microbiome responses following F0-F1 host shift and the importance of local effects which heavily affected the diversity and composition of microbiomes. We identified the main bacterial genera responsible for differences between treatments and provided a first overview of the metabolic pathways in which they are involved. These data further stress the importance of a careful approach when drawing general inferences based on laboratory populations or from non-adequately replicated field samples.