Immunoglobulin D (IgD) is an ancient antibody with dual membrane-bound and fluid-phase antigen receptor functions. The biology of secreted IgD remains elusive. Here, we demonstrate that teleost IgD+IgM− plasmablasts constitute a major lymphocyte population in some mucosal surfaces, including the gut mucosa. Remarkably, secreted IgD binds to gut commensal bacteria, which in turn stimulate IgD gene transcription in gut B cells. Accordingly, secreted IgD from gut as well as gill mucosae, but not the spleen, show a V(D)J gene configuration consistent with microbiota-driven clonal expansion and diversification, including mild somatic hypermutation. By showing that secreted IgD establishes a mutualistic relationship with commensals, our findings suggest that secreted IgD may play an evolutionary conserved role in mucosal homeostasis. Display omitted •IgD+IgM− B cells constitute the main non-IgT B cell subset in rainbow trout guts•Gut IgD responses establish a two-way interaction with the local microbiota•Mucosal but not splenic IgD undergoes clonal expansion and diversification•Despite the lack of germinal centers, mucosal IgD is mildly mutated in rainbow trout Perdiguero et al. show that IgD+IgM− plasmablasts constitute a major lymphocyte population in the teleost intestine, as in gills. In these two tissues, IgD molecular signatures reflect a clonal expansion not detected in the spleen. Finally, secreted IgD in the intestine establishes a two-way interaction with the local microbiota.