Abstract B cells express both an adaptive antigen-specific B cell receptor (BCR) and innate Toll-like receptors (TLRs) allowing the functional outcome of the B cell’s engagement with antigen to be modulated in response to pathogen-derived TLR ligands. In T cell-dependent responses, the BCR both signals for B cell proliferation and differentiation and also internalizes bound antigen for processing and presentation to helper T cells. Here we show that although the presence of the TLR9 ligand, CpG, does not affect early BCR mediated events following antigen binding including phosphorylation of key components of the signaling cascade and the formation of BCR clusters on cell surface, CpG alters the outcome of BCR signaling, resulting in unique transcriptional profiles, enhanced proliferation and differentiation to antibody secreting cells. In contrast, CpG dramatically limits the ability of B cells to process and present antigen to helper T cells. In the presence of CpG, BCR-induced upregulation of CD86 and MHC class II expressions are antagonized and antigen internalized by the BCR is not properly trafficked to antigen processing compartments resulting in reduced numbers of peptide-MHC class II complexes on the B cell surface. Indeed, CpG treated antigen-specific B cells show a reduced ability to maintain contact with antigen-specific T cells and to activate antigen-specific helper T cell proliferation in vitro. These results suggest that TLR9 activation in T cell dependent responses would drive B cell toward proliferation and antibody secretion and away from events that are highly dependent on the ability of B cells to present antigen to helper T cells, such as entry into germinal centers and affinity selection.