Although 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 oral RV infection induces gut-resident LLPCs that produce highly mutated protective IgA. Unlike RV-specific IgG + LLPCs, IgA + LLPCs were generated independently of MHCII expression by dendritic cells - rather MHCII expression by B cells was both necessary and sufficient. B cell MHCII was also sufficient to induce a unique population of T-bet + follicular helper T (T FH 1) cells which were crucial for RV-specific IgA + LLPC accumulation in the gut via IFNγ- and CXCR3-dependent mechanisms. Similar to RV infection, T FH 1 cells were required for influenza-specific IgA response. However, unlike RV infection, B cell MHCII 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 T FH 1 cells support IgA responses to mucosal viral infections.