G protein-coupled receptors do not only feature the orthosteric pockets, where most endogenous agonists bind, but also a multitude of other allosteric pockets that have come into the focus as potential binding sites for synthetic modulators. We have investigated 557 GPCR structures to better characterise such pockets by exhaustively docking small molecular probes in silico and converting the ensemble of binding locations to pocket-defining volumes. Our analysis confirmed all previously identified pockets and revealed nine previously untargeted sites. In order to test for the feasibility of functional modulation of receptors through binding of a ligand to such sites, we mutated residues in two sites in two model receptors. Moreover, we analysed the correlation of inter-residue contacts with the activation states of receptors and showed that contact patterns closely correlated with activation indeed coincide with these sites.