The B-cell antigen receptor (BCR) is composed of a membrane-bound immunoglobulin (mIg) of class M, D, G, E or A for antigen recognition1–3 and a disulfide-linked Igα and Igβ heterodimer (Igα/β) that functions as the signalling entity through their intracellular immunoreceptor tyrosine-based activation motifs (ITAMs)4,5. The organizing principle of the BCR remains elusive. Here we report cryogenic electron microscopy structures of mouse full-length IgM BCR at 8.2 Å resolution and its Fab-deleted form at 3.3 Å resolution. At the ectodomain (ECD), the Igα/β heterodimer mainly uses Igα to associate with Cµ3-Cµ4 domains of one heavy chain (µHC) while leaving the other heavy chain (µHC’) empty. The transmembrane domain (TMD) helices of the two µHCs interact with those of the Igα/β heterodimer to form a tight 4-helix bundle. The asymmetry at the TMD prevents the recruitment of two Igα/β heterodimers. Surprisingly, the connecting peptide between the ECD and TMD of µHC intervenes in between those of Igα and Igβ to guide the TMD assembly through striking charge complementarity. Weaker but distinct density for the Igβ ITAMs nestles next to the TMD, suggesting potential autoinhibition of ITAM phosphorylation. Interfacial analyses suggest that all BCR classes utilize a general organizational architecture. Our studies provide a structural platform for understanding B-cell signalling and designing rational therapies against BCR-mediated diseases.