Antibodies that define the Lancefield Streptococcus Group A (GAS) react with N-Acetyl-Glucosamine (GlcNAc) residues of the immunodominant Group A Carbohydrate (GAC). GlcNAc epitopes are not restricted to GAS, and GlcNAc-reactive Abs bind to a variety of glycans incorporating this amino-sugar. In mice, the GlcNAc-reactive B cell compartment requires commensal microbiota, demonstrating that non-GAS antigens contribute to the GAC-responsive B cell repertoire. To evaluate the ontogeny of GlcNAc-focused humoral immunity in humans, we utilized GAS GAC preparations as a high-fidelity antigen label and generated ~300 recombinant Abs from GAC-binding B cells derived from five pediatric tonsils (0-5 years of age). GAC-reactive Abs displayed remarkable diversity in their fine specificity toward GlcNAc and hexosamine containing structures. Clustering the reactivities of GAC-reactive Abs revealed several distinct specificity clades present in all samples but encoded by patient specific BCR sequences. Using 10x single-cell transcriptomics, we confirmed that GAC-reactive B cells were enriched in cells bearing germinal center (GC) B signatures. 10x immunoglobulin VDJ sequencing further revealed multiple expanded clonotypes diversified by somatic mutation. Comparing the reactivity of the consensus of these clonotypes with that of their unmutated common ancestor, we confirmed that GlcNAc-reactive B cells are affinity maturated. Collectively these data demonstrate that GAC-reactive Ab emerge early in life, are derived from mucosa-associated GCs, where they undergo clonal expansion and affinity maturation. Thus, the human GAC-reactive B cell repertoire is comprised of a collection of diverse private clonotypes, shaped by antigen-selection and affinity maturation, which converge onto multiple discrete reactivities toward carbohydrate antigens.