Newborns are highly susceptible to pathogenic infections with significant worldwide morbidity possibly due to an immature immune system. Recently, we reported that Propionibacterium strain, P. UF1, isolated from the gut microbiota of preterm infants, induced the differentiation of bacteria-specific Th17 cells. Here, we demonstrate that P. UF1 significantly increased the number of protective Th17 cells and maintained IL-10+ regulatory T cells (Tregs) in newborn mice. In addition, P. UF1 protected mice from intestinal Listeria monocytogenes (L. m) infection. P. UF1 also functionally sustained the gut microbiota and induced critical B vitamin metabolites implicated in the regulation of T cell immunity during L. m intestinal infection. Transcriptomic analysis of P. UF1-induced Th17 cells revealed genes involved in the differentiation and regulation of these cells. These results illustrate the potency of P. UF1 in the enhancement of neonatal host defense against intestinal pathogen infection.