Although tissue-resident memory T cells (T_RM cells) are critical in fighting infection, their fate after local pathogen re-encounter is unknown. Here we found that skin T_RM cells engaged virus-infected cells, proliferated in situ in response to local antigen encounter and did not migrate out of the epidermis, where they exclusively reside. As a consequence, secondary T_RM cells formed from pre-existing T_RM cells, as well as from precursors recruited from the circulation. Newly recruited antigen-specific or bystander T_RM cells were generated in the skin without displacement of the pre-existing T_RM cell pool. Thus, pre-existing skin T_RM cell populations are not displaced after subsequent infections, which enables multiple T_RM cell specificities to be stably maintained within the tissue.