Maternal obesity during pregnancy is associated with an increased risk of neurodevelopmental disorders, including autism spectrum disorder (ASD). This study investigates the impact of maternal high-fat diet (MHFD) on the offspring's social behavior and gut microbiota. Offspring from MHFD mothers exhibit social deficits and gut microbiota dysbiosis. These deficits can be prevented by co-housing with offspring from mothers on a regular diet (MRD) or by transferring their gut microbiota to germ-free mice. Social interaction induces synaptic potentiation in the ventral tegmental area (VTA) of MRD offspring but not MHFD offspring. MHFD offspring also have fewer oxytocin-immunoreactive neurons in the hypothalamus. Using metagenomics and precision microbiota reconstitution, the study identifies *Lactobacillus reuteri* as a single commensal strain that corrects oxytocin levels, synaptic function, and social deficits in MHFD offspring. Probiotic treatment with *L. reuteri* may offer a potential non-invasive treatment for neurodevelopmental disorders, including ASD.Maternal obesity during pregnancy is associated with an increased risk of neurodevelopmental disorders, including autism spectrum disorder (ASD). This study investigates the impact of maternal high-fat diet (MHFD) on the offspring's social behavior and gut microbiota. Offspring from MHFD mothers exhibit social deficits and gut microbiota dysbiosis. These deficits can be prevented by co-housing with offspring from mothers on a regular diet (MRD) or by transferring their gut microbiota to germ-free mice. Social interaction induces synaptic potentiation in the ventral tegmental area (VTA) of MRD offspring but not MHFD offspring. MHFD offspring also have fewer oxytocin-immunoreactive neurons in the hypothalamus. Using metagenomics and precision microbiota reconstitution, the study identifies *Lactobacillus reuteri* as a single commensal strain that corrects oxytocin levels, synaptic function, and social deficits in MHFD offspring. Probiotic treatment with *L. reuteri* may offer a potential non-invasive treatment for neurodevelopmental disorders, including ASD.