The following steps of telomere evolution are proposed. (i) In the proto-eukaryotic organism, the linearization of the genome by group II intron is initially accompanied by the D-loop mediated, BIR-like extension of the strand bearing the 3’ end. In addition, Pol α was enlisted from a virus to mediate C-strand synthesis, Concurrently, the archaeal-eukaryal RPA may have duplicated and given rise to the proto-CST complex (CST*) capable of regulating primase-Pol α. (ii) Subsequently, telomerase evolved from group II intron or a related reverse transcriptase to mediate the synthesis of short telomere repeats in cooperation with telomerase RNA. The proto-CST (CST*) has the necessary localization and DNA-binding property to also regulate telomerase at this stage of telomere evolution. (iii) Finally, the proto-CST underwent another round of duplication to give rise to PT–the proto-TEN1 was either not duplicated or lost during evolution. CST and PT underwent sub- and neofunctionalization such that PT acquired the ability to interact with other shelterin proteins and to specialize in the recruitment and activation of telomerase.