Background: Epidermal-resident memory CD8 ⁺ T (T _RM) cells play a significant role in fighting off pathogens. However, CD8 ⁺ T _RM cells are also central in the pathogenesis of a variety of inflammatory skin diseases. It is unclear whether the generation and persistence of CD8 ⁺ T _RM cells are dependent on the presence of cognate antigen and T cell receptor (TCR) signaling. Methods: We determined the generation and persistence of epidermal CD8 ⁺ T _RM cells by flow cytometry and single-cell TCR sequencing in a well-characterized mouse model for allergic contact dermatitis. We examined the responses to four different contact allergens in combination with adoptive transfer and prime-pull experiments. We determined the presence of contact allergens in the skin by Western blot analysis. Results: We found that epidermal CD8 ⁺ T _RM cells can develop in the absence of the cognate antigen and TCR signaling as determined by Nur77 induction, whereas persistence of epidermal CD8 ⁺ T _RM cells requires presence of the cognate antigen and correlates with Nur77 expression. In the presence of contact allergen, a selective expansion of specific TCR clonotypes was seen. Conclusion: This study demonstrates that cognate antigen and TCR signaling are required for the persistence of allergen-specific CD8 ⁺ T _RM cells in the skin.