Positive selection and plasma cell differentiation of high affinity germinal centre (GC) B cells delivers the protective antibodies responsible for long-term humoral immunity after infection and vaccination. Within GCs, dark zone (DZ) B cells undergo intense proliferation and somatic hypermutation (SHM) of their antigen receptor (BCR) variable region genes before migrating to the GC light zone (LZ). Once in the LZ, B cells: i) are exposed to antigen displayed in immune complexes on the surface of follicular dendritic cells (FDCs), and ii) present BCR-internalized and processed antigen to CD4+ T follicular helper (TFH) cells. It is well established that LZ B cells that have acquired high affinity BCRs are preferentially selected to undergo further rounds of SHM in the DZ or differentiate directly into antibody-secreting plasma cells. What remains controversial, however, is the specific mechanism whereby expression of a high affinity BCR translates into positive selection or plasma cell differentiation. Here we use a high-resolution model of GC selection and differentiation to show that it is the acute delivery of signals to high-affinity GC B cells upon their interaction with antigen that provides the fundamental stimulus for both positive selection and plasma cell differentiation. In contrast, signals from TFH cells are not linked with sufficient precision to GC B cell affinity to preferentially stimulate high affinity clones and supported the activation and DZ migration of low affinity LZ B cells. These data establish that competition for antigen-dependent signals rather than TFH cell help is the primary driver of the affinity maturation of protective antibody responses.