Summary Background We have previously shown that maternal cow's milk (CM) elimination results in downregulation of CM‐specific IgA antibody levels in BM, but not in serum, suggesting that an entero‐mammary link may exist for food‐specific antibody‐secreting cells. Objective We sought to investigate whether food‐specific IgA epitope profiles differ intra‐individually between mother's serum and BM. We also examined how infants’ food epitope‐specific IgA develops in early infancy and the relationship of IgA epitope recognition with development of cow's milk allergy (CMA). Methods We measured specific IgA to a series of overlapping peptides in major CM allergens (αs1‐, αs2‐, β‐ and κ‐caseins and β‐lactoglobulin) in paired maternal and infant serum as well as BM samples in 31 mother‐infant dyads within the first 15 post‐partum months utilizing peptide microarray. Results There was significant discordance in epitope specificity between BM and maternal sera ranging from only 13% of sample pairs sharing at least one epitope in αs1‐casein to 73% in κ‐casein. Epitope‐specific IgA was detectable in infants’ sera starting at less than 3 months of age. Sera of mothers with a CMA infant had increased binding of epitope‐specific IgA to CM proteins compared to those with a non‐CMA infant. Conclusion & Clinical Relevance These findings support the concept that mother's milk has a distinct antifood antibody repertoire when compared to the antibody repertoire of the peripheral blood. Increased binding of serum epitope‐specific IgA to CM in mothers of infants with CMA may reflect inherited systemic immunogenicity of CM proteins in these families, although specific IgA in breast milk was not proportionally up‐regulated.