CD4 T follicular helper (Tfh) cells are a crucial component of germinal centre (GC) reactions-mediated humoral immune responses. However, the regulation of protective Tfh-GC responses during the type 2 response to intestinal helminths remains poorly characterized. Here we use the helminth parasite Trichuris muris (T. muris) that allows us to evaluate Tfh-GC responses and their roles during Th1-associated susceptibility and Th2-dependent protective response. We show that a diminished Tfh-GC B cell response is associated with Th1-mediated chronic T. muris infection. In contrast, Th2-induced acute T. muris infection promotes robust Tfh-GC responses, which correlates with type 2 protective immunity to infection. Acute-induced Tfh cells express GATA3 and IL-4, whereas IFN-γ and T-bet expression are mainly observed in chronic-induced Tfh cells. Transcriptomic and epigenetic landscape analysis reveals that acute and chronic T. muris infection promotes Th2- and Th1-like Tfh cells, respectively. Blockade of GC-dependent Th2-like Tfh cell response during acute T. muris infection promotes chronic infection, which is consistent with the transfer of Th2-like Tfh cells that promotes type 2-mediated resistance to chronic infection. Collectively, our results provide insights into the protective roles of Tfh-GC response during helminth infection and identify distinct functional, transcriptional, and epigenetic features of Tfh cells that emerge during resolving or chronic helminth infections.