People residing in endemic areas of malaria develop immunity against clinical symptoms of Plasmodium infection after years of repeated exposure. The reasons for this are poorly understood to date; however, an increasing number of immuno-epidemiological studies in high malaria transmission areas indicate that antibodies and memory B cells that provide humoral immunity, are acquired inefficiently and short-lived. In contrast, long-lived memory B cells can be generated after a few symptomatic infections in low transmission settings. This suggests that acute infection may impede the development of humoral immunity. In support of this, pro-inflammatory responses induced by blood-stage malaria infection have been revealed to impair humoral immunity in mice by inhibiting the germinal centre response, which is critical for the establishment of B cell memory. To delineate the underlying molecular mechanism, we investigated the role of the pro-inflammatory, T helper 1 transcription factor T-bet, in regulating germinal centre development during blood-stage P. berghei ANKA infection. We found that genetic ablation of T-bet in mixed bone marrow chimeric mice restored the formation of germinal centres in the spleen and enhanced the production of parasite-specific antibodies. CD4 T cell upregulation of T-bet during infection strikingly inhibited the differentiation of T follicular helper cells, which consequently compromised the germinal centre and plasma cell response. T-bet up-regulation during infection not only affected CD4+ T cell help, but interestingly, also directly affected B cell differentiation. T-bet expression by B cells suppressed the expansion of the germinal centre response, and further modulated its cellular dynamics and maturation. We reveal that the pro-inflammatory response mediated by T-bet during acute infection regulates the acquisition of humoral immunity to malaria. This knowledge is crucial for the development of next generation vaccines and immunotherapies that induce sustained humoral immune protection against malaria.