Allosteric modulation of cannabinoid receptor type 1 (CB1R) offers a promising alternative to conventional therapeutic approaches using orthosteric ligands (OLs). Currently, CB1R allosteric modulators (AMs) are characterized based on their ability to modulate binding or functional response of OLs, preventing isolation of individual contributions by allosteric and orthosteric ligands. Herein, we develop the first allosteric fluoroprobe and attendant FRET-based assay allowing for the direct profiling of CB1R AMs without coincubation with an OL. Our allosteric tracer enables differentiation of allosteric and orthosteric ligands as well as their pharmacological profiling at CB1R. The utility of this work is highlighted by addressing ambiguities surrounding the binding of cannabidiol (CBD). CBD was found to interact with both allosteric and orthosteric sites of CB1R with comparable affinity (pKi = 5.34 and 5.67, respectively).