Telomere maintenance in eukaryotes is linked to cellular proliferation capacity. The telomerase holoenzyme, which maintains telomere length, is a central actor in this process and its function is highly conserved among eukaryotes. Telomerase is a ribonucleoproteic complex constituted of an RNA template and proteic subunits with catalytic and regulatory activities. Several factors required for the activity and recruitment of telomerase at telomeres have been identified in the past years. However, it is still poorly understood how this holoenzyme is assembled in cells. Recent studies in mammalian and yeast cells have underscored the importance of telomerase RNA trafficking in telomerase biogenesis and telomere homeostasis. These studies revealed that telomerase biogenesis is a highly dynamic process, which is regulated in space and time, and which ultimately affects how cells maintain genome integrity.