A comprehensive analysis of cellular and molecular drivers of bone marrow microenvironmental aging, particularly those involving repetitive transposable elements, has been lacking. By integrating single-cell multiomics with a deep learning framework, SenNet, we identified senescent mesenchymal stromal cells (MSCs) in mouse and human bone marrow that accumulate senescence-associated secretory phenotype (SASP) factors during aging and hematological malignancies. We discovered a distinct class of senescence chromatin-activated retrotransposons (SCARs), including RLTR6/MMVL30, a group of young ERV1 endogenous retroviruses, that are epigenetically silenced by EZH2 in proliferating MSCs but become selectively activated in senescent MSCs through AP-1-mediated enhancer-promoter rewiring. SCAR activation triggers pro-inflammatory cascades within the bone marrow stromal microenvironment, whereas genetic or pharmacologic inhibition of the AP-1-SCAR-cGAS/STING axis suppresses SASP production in senescent MSCs, thereby alleviating hematopoietic aging and leukemia progression. Collectively, these findings establish SCAR-mediated inflammatory signaling in the stromal microenvironment as a critical driver of hematopoietic aging and malignancy.