G protein-coupled receptors (GPCRs) are essential mediators of cellular communication. Highlighting their utmost biomedical significance, over 1000 structures of GPCRs in complex with coupling partners have been reported. However, the overwhelming majority of published structures are in complex with G proteins. Beyond G proteins, GPCRs interact with a variety of intracellular partners, and structural information with these other proteins is comparatively scarce. Among these other partners are arrestin proteins, which bind most GPCRs and are associated with signal termination and receptor trafficking. Here, we report the first structure of a class B1 GPCR, the parathyroid hormone receptor (PTH1R), bound to beta-arrestin-2. Compared to structures of PTH receptor with G proteins, there is markedly higher flexibility between the receptor and arrestin, which necessitated extensive classification to resolve the conformational heterogeneity. Our structure revealed that arrestin’s crucial “finger loop” accesses the core of the activated receptor, which adopts a subtly distinct conformation compared to that of a G protein-bound state. One of the receptor’s three intracellular loops forms a key binding interface with arrestin. Overall, our structure provides insights into the molecular basis of signaling regulation for class B1 GPCRs and lays foundations for the development of agonists that selectively target different coupling partners.