The participation of dendritic cells (DCs) in CD8⁺ T‐cell‐mediated allograft rejection is a long‐standing question of great clinical relevance for tissue transplantation. Here, we show that Batf3^−/− mice demonstrate delayed allo‐skin graft rejection and are deficient in priming allo‐specific CD8⁺ T cells. Batf3^−/− mouse priming is restored by transferring either purified CD8α⁺ or CD103⁺ DCs, demonstrating the critical role of these cells in alloreactivity. Using D^b‐restricted antiviral F5 transgenic T‐cell receptor T cells, which we demonstrate are alloreactive with H‐2K^d, we show that cross‐dressing of CD8α⁺ and CD103⁺ primes CD8⁺ T‐cell or allo‐specific responses in vitro and in vivo. These findings suggest novel strategies for moderating tissue rejection based on interfering with DC cross‐dressing or subsequent interaction with T cells.