Abstract The skin is one of the largest barrier sites which harbors a plethora of microorganisms. Whether skin microbiota promotes humoral responses remains unknown. Here we show that colonization with common skin commensal Staphylococcus epidermidis profoundly modulates cutaneous immunity that results in serum responsiveness with antigen-specific IgG antibodies. Such response is uncoupled from inflammatory signals and is associated with the induction of dermal tertiary lymphoid organs that closely resemble classical germinal centers. Of note, such responses occur in a tissue autonomous manner as evidenced by the preserved antibody repertoire in mice deficient in professional lymphoid organs. Our data also uncover a non-redundant role for Langerhan’s cells for the generation of commensal specific antibodies. Further, our work proposes a model by which commensal specific antigens are collected in the hair follicle leading to the generation of T follicular helper cells that further expand the local B cell pool in an IL-21-dependent manner. We also found that commensal induced antibodies can protect the host against subsequent infection with the same microbe demonstrating the importance of this line of defense in maintaining barrier protection. Collectively, our observations highlight the autonomous potential of skin organizational flexibility and for the first time demonstrate that B cells represent an indispensable local cutaneous compartment that actively maintains skin immunity.