It has been hypothesized that G-quadruplexes can sequester the 3' end of the telomere and prevent it from being extended by telomerase. Here we purify and characterize stable， conformationally homogenous human telomeric G-quadruplexes， and demonstrate that human telomerase is able to extend parallel， intermolecular conformations in vitro. These G-quadruplexes align correctly with the RNA template of telomerase， demonstrating that at least partial G-quadruplex resolution is required. A highly purified preparation of human telomerase retains this extension ability， establishing that the core telomerase enzyme complex is sufficient for partial G-quadruplex resolution and extension. The parallel-specific G-quadruplex ligand N-methyl mesoporphyrin IX (NMM) causes an increase in telomeric G-quadruplexes， and we show that telomerase colocalizes with a subset of telomeric G-quadruplexes in vivo. The ability of telomerase to partially unwind， extend and localize to these structures implies that parallel telomeric G-quadruplexes may play an important biological role.