During the evolution of linear genomes, it became essential to protect the natural chromosome ends to prevent triggering of the DNA-damage repair machinery and enzymatic attack. Telomeres — tightly regulated complexes consisting of repetitive G-rich DNA and specialized proteins — accomplish this task. Telomeres not only conceal linear chromosome ends from detection and inappropriate repair but also provide a buffer to counteract replication-associated shortening. Lessons from many model organisms have taught us about the complications of maintaining these specialized structures. Here, we discuss how telomeres interact and cooperate with the DNA replication and DNA-damage repair machineries.