CD8+ tissue-resident memory T cells (T RM cells) reside permanently in nonlymphoid tissues and provide a first line of protection against invading pathogens. However, the precise localization of CD8+ T RM cells in the lung, which physiologically consists of a markedly scant interstitium compared with other mucosa, remains unclear. In this study, we show that lung CD8+ T RM cells localize predominantly in specific niches created at the site of regeneration after tissue injury, whereas peripheral tissue-circulating CD8+ effector memory T cells (T EM cells) are widely but sparsely distributed in unaffected areas. Although CD69 inhibited sphingosine 1–phosphate receptor 1–mediated egress of CD8+ T cells immediately after their recruitment into lung tissues, such inhibition was not required for the retention of cells in the T RM niches. Furthermore, despite rigid segregation of T EM cells from the T RM niche, prime-pull strategy with cognate antigen enabled the conversion from T EM cells to T RM cells by creating de novo T RM niches. Such damage site–specific localization of CD8+ T RM cells may be important for efficient protection against secondary infections by respiratory pathogens.