The transcriptional repressor Bcl-6 is linked to the development of both CD4⁺ T follicular helper (T_FH) and central memory T (T_CM) cells. Here, we demonstrate that in response to decreased IL-2 signalling, T helper 1 (T_H1) cells upregulate Bcl-6 and co-initiate T_FH- and T_CM-like gene programs, including expression of the cytokine receptors IL-6Rα and IL-7R. Exposure of this potentially bi-potent cell population to IL-6 favours the T_FH gene program, whereas IL-7 signalling represses T_FH-associated genes including Bcl6 and Cxcr5, but not the T_CM-related genes Klf2 and Sell. Mechanistically, IL-7-dependent activation of STAT5 contributes to Bcl-6 repression. Importantly, antigen-specific IL-6Rα⁺IL-7R⁺ CD4⁺ T cells emerge from the effector population at late time points post influenza infection. These data support a novel role for IL-7 in the repression of the T_FH gene program and evoke a divergent regulatory mechanism by which post-effector T_H1 cells may contribute to long-term cell-mediated and humoral immunity.