The gut microbiome of insects directly or indirectly affects the metabolism, immune status, sensory perception and feeding behavior of its host. Here, we examine the hypothesis that in the oriental fruit fly (Bactrocera dorsalis, Diptera: Tephritidae), the presence or absence of gut symbionts affects foraging behavior and nutrient ingestion. We offered protein-starved flies, symbiotic or aposymbiotic, a choice between diets containing all amino acids or only the non-essential ones. The different diets were presented in a foraging arena as drops that varied in their size and density, creating an imbalanced foraging environment. Suppressing the microbiome resulted in significant changes of the foraging behavior of both male and female flies. Aposymbiotic flies responded faster to the diets offered in experimental arenas, spent more time feeding, ingested more drops of food, and were constrained to feed on time-consuming patches (containing small drops of food), when these offered the full complement of amino acids. We discuss these results in the context of previous studies on the effect of the gut microbiome on host behavior, and suggest that these be extended to the life history dimension. © 2019 Akami et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.