The increasing prevalence of food allergies has been causally associated with the depletion of allergy protective intestinal bacteria. However, few studies have investigated the role of the gut microbiota in promoting allergic responses. In a cohort of cow’s milk allergic (CMA) infants, we have identified a patient with a proinflammatory and atopic microbiota. In comparison to a healthy microbiota, this CMA microbiota has increased abundance of Bacteroidetes, a Gram-negative phylum of bacteria that has been associated with increased incidence of atopy. Using this microbiota, we investigated the host-microbe interactions that mediate these intestinal inflammatory responses. To examine these interactions, we used mice with global and conditional abrogation in TLR4 signaling, as Gram-negative bacteria signal through this receptor via membrane-derived lipopolysaccharide (LPS). We show that this donor’s microbiota induces serum amyloid A1 (Saa1) and other Th17-, B cell-, and Th2-associated genes in the ileal epithelium. Accordingly, this microbiota also induces Th17 cells, as well as regulatory T cell populations and fecal IgA. Importantly, we used both antibiotic-treated SPF and rederived germ-free mice with a conditional mutation of TLR4 in the CD11c+ compartment to demonstrate that the induction of proinflammatory genes, fecal IgA, and Th17 cells is dependent on TLR4 signaling. Furthermore, metagenomic sequencing revealed that the CMA microbiota also has increased abundance of LPS biosynthesis, which is likely derived from Bacteroidetes. Lastly, upon sensitization with β-lactoglobulin, this CMA microbiota induces a TLR4-dependent mixed type 2/type 3 response in innate lymphoid cells (ILCs) during the early phases of allergic sensitization. Taken together, our results show that a Bacteroidetes-enriched microbiota with increased abundance of LPS genes promotes a mixed Th17/Th2 response in a subset of infants with cow’s milk allergy.