The role of different DC subsets in priming and maintenance of immunity against Leishmania major (L. major) infection is debated. The transcription factor basic leucine zipper transcription factor, ATF‐like 3 (Batf3) is essential for the development of mouse CD103⁺ DCs and some functions of CD8α⁺ DCs. We found that CD103⁺ DCs were significantly reduced in the dermis of Batf3‐deficient C57BL/6 mice. Batf3^−/− mice developed exacerbated and unresolved cutaneous pathology following a low dose of intradermal L. major infection in the ear pinnae. Parasite load was increased 1000‐fold locally and expanded systemically. Batf3 deficiency did not affect L. major antigen presentation to T cells, which was directly exerted by CD8α⁻ conventional DCs (cDCs) in the skin draining LN. However, CD4⁺ T‐cell differentiation in the LN and skin was skewed to nonprotective Treg‐ and Th2‐cell subtypes. CD103⁺ DCs are major IL‐12 producers during L. major infection. Local Th1 immunity was severely hindered, correlating with impaired IL‐12 production and reduction in CD103⁺ DC numbers. Adoptive transfer of WT but not IL‐12p40^−/− Batf3‐dependent DCs significantly improved anti‐L. major response in infected Batf3^−/− mice. Our results suggest that IL‐12 production by Batf3‐dependent CD103⁺ DCs is crucial for maintenance of local Th1 immunity against L. major infection.