Although tissue-resident memory T cells (T cells) are critical in fighting infection， their fate after local pathogen re-encounter is unknown. Here we found that skin T 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 cells formed from pre-existing T cells， as well as from precursors recruited from the circulation. Newly recruited antigen-specific or bystander T cells were generated in the skin without displacement of the pre-existing T cell pool. Thus， pre-existing skin T cell populations are not displaced after subsequent infections， which enables multiple T cell specificities to be stably maintained within the tissue.