Photosynthetic organisms protect themselves from high-light stress by dissipating excess absorbed energy as heat in a process called non-photochemical quenching (NPQ). Zeaxanthin is essential for the full development of NPQ, but its role remains debated. The main discussion revolves around two points: where does zeaxanthin bind and does it quench? To answer these questions we have followed the zeaxanthin-dependent quenching from leaves to individual complexes, including supercomplexes. We show that small amounts of zeaxanthin are associated with the complexes, but in contrast to what is generally believed, zeaxanthin binding per se does not cause conformational changes in the complexes and does not induce quenching, not even at low pH. We show that in NPQ conditions zeaxanthin does not exchange for violaxanthin in the internal binding sites of the antennas but is located at the periphery of the complexes. These results together with the observation that the zeaxanthin-dependent quenching is active in isolated membranes, but not in functional supercomplexes, suggests that zeaxanthin is acting in between the complexes, helping to create/participating in a variety of quenching sites. This can explain why none of the antennas appears to be essential for NPQ and the multiple quenching mechanisms that have been observed in plants.