To address this problem we have utilized single-molecule Förster Resonance Energy Transfer (FRET) microscopy in combination with molecular dynamics (MD) simulations. Single-molecule FRET microscopy allows real-time monitoring of the folding of single G4 molecules, omitting both time and population averaging (31) and thus provides a direct view of G4 conformational diversity and dynamics. Whereas, combining the single-molecule FRET data with MD simulations allowed obtaining the structural description of the experimentally observed G4 states. We find that the hybrid 1 conformation represents the predominant long-lived folded conformation of the human telomeric sequence in potassium containing solutions. Before reaching this conformation, several alternative off-pathway folding transitions occur into marginally stable anti-parallel chair, 2-tetrad anti-parallel basket and hybrid 2 conformations.