Tissue-resident memory T (TRM) cells are a stable population of non-recirculating immune cells that accumulate and persist in peripheral tissues including the skin. Whereas skin CD8+ TRM cells producing cytokines such as IFNγ (Tc1) are known to be critical for protection against peripheral infections and solid cancers, alternate subsets of IL-17-producing skin CD8+ (Tc17) TRM cells have been implicated in wound healing as well as autoimmune disorders including psoriasis. Whether these skin Tc1 and Tc17 TRM cells depend on similar factors for their formation and survival is currently unclear. Topical colonisation of mice with the human commensal bacterium Staphylococcus epidermidis induces formation of distinct Tc1 and Tc17 TRM cell populations resembling those found in human skin. Using this model, we show that Tc1 and Tc17 skin TRM cells differentially depend upon key cytokines and transcription factors implicated in tissue residency and T cell survival. Moreover, targeting cytokine signalling pathways and surface molecules specifically upregulated in Tc17 TRM cells permitted selective ablation of the Tc17 TRM cell subset from skin without depleting Tc1 TRM cells. Our work indicates that functionally distinct TRM cells residing in a single given tissue can exhibit unappreciated phenotypic heterogeneity and diverse developmental and survival requirements. As such, our findings highlight novel strategies through which Tc17 TRM cells might be specifically targeted without perturbing Tc1 TRM cell populations. Ultimately, this information may inform design of future immunotherapies that could possibly be used to treat autoimmune disorders associated with CD8+ TRM cells without compromising anti-pathogen and cancer immunity.