Although immunoglobulin A (IgA)+ long-lived plasma cells (LLPCs) generated following mucosal viral infection provide durable protection against reinfection, little is known about their generation. Here, we show that rotavirus (RV) infection induces gut-resident LLPCs that produce highly mutated, protective IgA. Unlike RV-specific immunoglobulin G (IgG)+ LLPCs, IgA+ LLPCs were generated independently of major histocompatibility complex class II (MHC class II) expression by dendritic cells-rather, MHC class II on B cells was both necessary and sufficient. B cell-MHC class II was also sufficient to induce T-bet+ follicular helper T (TFH1) cells, which were crucial for RV-specific IgA+ LLPC accumulation in the gut via interferon γ (IFNγ)- and CXCR3-dependent mechanisms. Similar to RV infection, TFH1 cells were required for an influenza-specific IgA response in the airway. However, unlike RV infection, B cell-MHC class II was not sufficient to induce influenza-specific IgA+ LLPCs, suggesting the operation of mucosal-site-specific priming mechanisms. Collectively, our data reveal that unconventionally primed TFH1 cells support IgA responses to mucosal viral infections.