The human proteome contains 826 G protein-coupled receptors (GPCR), which control a wide array of key physiological functions, making them important drug targets. GPCR functions are based on allosteric coupling from the extracellular orthosteric drug binding site across the cell membrane to intracellular binding sites for partners such as G proteins and arrestins. This signaling process is related to dynamic equilibria in conformational ensembles that can be observed by NMR in solution. A previous high-resolution NMR study of the A adenosine receptor (AAR) resulted in a qualitative characterization of a network of such local polymorphisms. Here, we used F-NMR experiments with probes at the AAR intracellular surface, which provides the high sensitivity needed for a refined description of different receptor activation states by ensembles of simultaneously populated conformers and the rates of exchange among them. We observed two agonist-stabilized substates that are not measurably populated in apo-AAR and one inactive substate that is not seen in complexes with agonists, suggesting that AAR activation includes both induced fit and conformational selection mechanisms. Comparison of AAR and a constitutively active mutant established relations between the F-NMR spectra and signaling activity, which enabled direct assessment of the difference in basal activity between the native protein and its variant.