Aging impairs tumor control by limiting CD8+ T cell function in the tumor microenvironment (TME). The study shows that the aged TME drives a unique dysfunctional state in CD8+ T cells, termed T_TAD, which is distinct from canonical T cell exhaustion. This state is characterized by reduced effector function, altered transcription, and epigenetic changes. The aged TME also impairs NK cell–dendritic cell (DC)–CD8+ T cell cross-talk, reducing CD8+ T cell priming by conventional type 1 DCs (cDC1s). Myeloid-targeted therapies that reinvigorate cDC1s can improve tumor control and restore CD8+ T cell immunity in aged mice. Aging reduces the infiltration of NK cells and cDC1s, which are critical for initiating robust CD8+ T cell responses, ultimately preventing aged mice from responding to mRNA neoantigen vaccines. The study highlights the importance of understanding the mechanisms limiting CD8+ T cell immunity in the aged TME and developing strategies to reinvigorate dysfunctional CD8+ T cells. The findings suggest that age-associated defects in CD8+ T cells and cDC1s restrict the ability of aged mice to respond to mRNA vaccines, and that myeloid-targeted immunotherapies, such as CD40 agonism, can rescue these defects and improve tumor control. The study also identifies a distinct age-associated T_TAD cell subset in human tumors, which is functionally and transcriptionally distinct from canonical exhausted CD8+ T cells. These findings have important implications for improving cancer immunotherapy outcomes in older individuals.Aging impairs tumor control by limiting CD8+ T cell function in the tumor microenvironment (TME). The study shows that the aged TME drives a unique dysfunctional state in CD8+ T cells, termed T_TAD, which is distinct from canonical T cell exhaustion. This state is characterized by reduced effector function, altered transcription, and epigenetic changes. The aged TME also impairs NK cell–dendritic cell (DC)–CD8+ T cell cross-talk, reducing CD8+ T cell priming by conventional type 1 DCs (cDC1s). Myeloid-targeted therapies that reinvigorate cDC1s can improve tumor control and restore CD8+ T cell immunity in aged mice. Aging reduces the infiltration of NK cells and cDC1s, which are critical for initiating robust CD8+ T cell responses, ultimately preventing aged mice from responding to mRNA neoantigen vaccines. The study highlights the importance of understanding the mechanisms limiting CD8+ T cell immunity in the aged TME and developing strategies to reinvigorate dysfunctional CD8+ T cells. The findings suggest that age-associated defects in CD8+ T cells and cDC1s restrict the ability of aged mice to respond to mRNA vaccines, and that myeloid-targeted immunotherapies, such as CD40 agonism, can rescue these defects and improve tumor control. The study also identifies a distinct age-associated T_TAD cell subset in human tumors, which is functionally and transcriptionally distinct from canonical exhausted CD8+ T cells. These findings have important implications for improving cancer immunotherapy outcomes in older individuals.