Autophagy dysfunction and senescence are established drivers of aging, but their interplay remains poorly understood. Here, we identify how the age-related decline in chaperone-mediated autophagy (CMA) affects properties and fate of senescent cells in old organisms. Cells with genetically downregulated CMA, mimicking its aging decline, still undergo senescence but display a distinct senescence-associated secretory phenotype, and proteomic and metabolic profiles phenocopying those in old senescent cells. Combined CMA decline in senescent cells and macrophages impair senescent cell clearance. In fact, macrophage-specific CMA blockage in mice is sufficient for senescent cell accumulation, highlighting a key role for macrophage CMA in their recognition and removal. Conversely, pharmacological CMA activation reduces senescent cell burden in old mice and disease severity in a pulmonary fibrosis mouse model. Our findings reveal a functional interplay between CMA decline and senescence cell persistence, highlighting CMA upregulation as a promising strategy to promote senescence resolution in old organisms.