Priming of CD8⁺ T cells specific for viruses that interfere with the MHC class I presentation pathway is a challenge for the immune system and is believed to rely on cross‐presentation. Cytomegalovirus (CMV) infection induces vigorous CD8⁺ T‐cell responses despite its potent immune evasion strategies. Furthermore, CD8⁺ T cells specific for a subset of viral epitopes accumulate and are maintained at high levels exhibiting an activated phenotype – referred to as “inflationary T cells”. Taking advantage Batf3^−/− mice in which the development of cross‐presenting CD8α⁺ and CD103⁺ DCs is severely compromised, we analyzed their role in the induction and inflation of murine (M)CMV‐specific CD8⁺ T‐cell responses. We found that priming of MCMV‐specific CD8⁺ T cells was severely impaired in the absence of cross‐presenting DCs. However, inflation of two immuno‐dominant MCMV‐specific CD8⁺ T‐cell populations was largely normal in the absence of cross‐presenting DCs, indicating that inflation during latency was mainly dependent on direct antigen presentation. These results highlight differential antigen presentation requirements during acute and latent MCMV infection.