Resident CD8⁺ DCs perform several functions, including cross‐presenting antigen and rapidly engulfing the Gram‐positive intracellular pathogen Listeria monocytogenes. Little is known about how these functions of CD8⁺ DCs are modulated. Here, we show that granulocyte‐macrophage CSF (GM‐CSF), a cytokine that exists at low levels at steady state but is elevated during infection and inflammation, enhances cross‐presentation and rapid uptake of L. monocytogenes by resident CD8⁺ DCs. This previously unrecognized functional enhancement of CD8⁺ DCs by GM‐CSF was independent of promoting DC survival in vitro. Enhancement of these functions by GM‐CSF was also marked by CD103 expression on CD8⁺ DCs that was strongly regulated by GM‐CSF. Our findings not only identify GM‐CSF as a key molecule regulating CD8⁺ DC function, but also as a factor responsible for functional heterogeneity of CD8⁺ DCs that is at least substantially demarcated by CD103 expression.