Although cancer is known to be predominantly a disease of the elderly, it is also thought that aging and cancer may occur either via similar or opposing cellular mechanisms. Studies during the past decades were focused on understanding the molecular events underlying both processes, aiming to ultimately improve the quality of life and lifespan. However, these efforts were traditionally performed or viewed independently without considering the interplay between aging and cancer-promoting mechanisms. Transforming growth factor-beta (TGF-β) signaling is essential for embryonic development and physiological tissue homeostasis. Although the fundamental roles of TGF-β in cancer progression have been investigated extensively, recent reports also provide evidence for its direct or indirect links to aging-related processes such as cell proliferation, senescence, stem cell renewal, DNA damage, inflammation, and telomere length. In this review, we present the latest findings regarding the TGF-β-regulated convergent and divergent mechanisms controlling the balance between aging and cancer. Finally, the implications of these processes in developing strategies to prolong the cancer-free human lifespan are discussed.