Gamma-ray observations with Imaging Atmospheric Cherenkov Telescopes (IACTs) are a unique probe for indirect detection of dark matter (DM) astrophysical signal. The scenario of TeV-scale Weakly Interactive Massive Particles - a compelling class of stable DM candidates - has been extensively explored using observations collected with the High Energy Stereoscopic System (H.E.S.S.), a hybrid array of five IACTs. After more than 20 years of stereoscopic observations, H.E.S.S. collected a variety of datasets from potential targets hosting DM with unprecedented sensitivity. Located in the Southern hemisphere, H.E.S.S. is in a privileged position to observe the Milky Way and the Galactic centre (GC) region. I will present the main results obtained with H.E.S.S. on the search for DM annihilation signals - considering also specific DM candidates like the Wino, Higgsino, and Quintuplet - from targets such as dwarf spheroidal galaxies, candidates DM subhalos in the Milky Way halo, and the GC region. These results establish a benchmark for the ultimate sensitivity of the current generation of IACT instruments to annihilating DM, providing conclusions directly relevant for searches of DM signals with the next generation of Cherenkov telescopes.