The germinal centre (GC) response is critical for both effective adaptive immunity and establishing peripheral tolerance by limiting autoreactive B cells. Dysfunction in these processes can lead to defective immune responses or contribute to autoimmune disease through the production of autoantibodies or ectopic GC structures. To understand the gene regulatory principles underlying the GC response and how common genetic variants may impact specific cellular states in autoimmune disease, we generated a single-cell transcriptomic and epigenomic atlas of the human tonsil, a widely studied and representative lymphoid tissue. In addition to characterizing diverse immune cell subsets and building a trajectory of dynamic gene expression and transcription factor activity during B cell differentiation, we leverage our cell type-specific transcriptomic and epigenomic maps to interpret potential regulatory impact of genetic variants implicated in autoimmunity, revealing that many non-coding genetic variants exhibit their greatest chromatin accessibility and regulatory potential in GC-associated cell populations. We also report examples of genetic variants associated with multiple autoimmune traits that exhibit chromatin accessibility across varied cellular populations, highlighting potentially pleiotropic mechanisms underlying their link with disease. Together, our analyses provide a powerful new immune cell type-resolved resource for the interpretation of cellular and genetic causes underpinning autoimmune disease.