The animal gut can be colonized by diverse microorganisms that impact the nutritional physiology of the animal host. Most research has concerned the effect of individual microorganisms, which may compete for dietary constituents, provide essential nutrients or modulate host signaling pathways regulating nutrient allocation and metabolic function. The goal of this dissertation was to investigate the effect of among-microbe interactions on the nutritional physiology of the animal host, using the Drosophila melanogaster gut microbiome as the experimental system. The specific aims were to 1) determine the genetic capacity for metabolic function of individual bacteria associated with Drosophila by genome sequence analysis, 2) investigate the effect of among-microbe interactions on Drosophila nutrient allocation and the underlying processes, and 3) assess the effect of microbial co-associations on the Drosophila metabolome. Results indicated that bacteria associated with Drosophila differ metabolically at multiple levels of taxonomy, from order to within-species, with redundant functions predicted to influence Drosophila performance and physiology. Complementary experimental studies using the bacteria Acetobacter fabarum and Lactobacillus brevis and yeast Hanseniaspora uvarum revealed that the nutritional traits of Drosophila vary both with the composition of the microbiota and between male and female flies. For example, the lipid content of male flies was negatively correlated with the titer of the microbial fermentation product acetic acid when the flies were co-associated with A. fabarum and H. uvarum. The metabolomic analysis of Drosophila provided evidence that the interaction between A. fabarum and L. brevis stimulates metabolic signaling to increase metabolic activity through the TCA cycle and for male flies, decrease glucose and lipid content. In addition, the microbial metabolite phenyllactic acid was identified as a statistically robust biomarker for low lipid content in Drosophila. Taken together, these studies reveal that nutritional traits of Drosophila are strongly influenced by the presence and composition of the gut microbiota, and that the effect of taxonomically-complex communities cannot be predicted from the traits of Drosophila bearing single microbial taxa. An imperative for future research is to determine the processes by which male and female hosts differ in their nutritional responses to microbial communities of different complexity and composition.