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As key targets for chronic pain, opioid receptors (ORs) are still at the forefront of drug discovery efforts. In the hunt for opioid analgesics that are free from adverse effects, recent high-throughput screening campaigns have focused on identifying allosteric modulators, that is molecules that bind non-conserved (allosteric) binding sites on the receptor, and modulate the potency and/or efficacy of ligands at the same (orthosteric) site as the endogenous agonist. Both positive and negative allosteric modulators (PAMs and NAMs) of μ-OR and δ-OR subtypes have recently been identified. While the recent crystal structures of ORs have revealed important details of ligand-receptor binding at the orthosteric site, both the location of allosteric sites on these receptors and the binding mode of opioid allosteric ligands are unknown. Here, we applied all-atom metadynamics to efficiently study the binding of a PAM and a NAM to the δ-OR in the presence of the orthosteric agonist SNC-80 and an explicit lipid-water environment. The dynamics of the allosteric ligands was enhanced by biasing the potential acting on the ligand-receptor distance, and a contact map reflecting the ligand-receptor interaction. The resulting energy landscapes show two deep energy minima for both the simulated PAM and NAM, which correspond to the ligands acquiring specific binding poses within two different nearby receptor pockets defined by transmembrane helices TM1, TM2, and TM7. Notably, the ligand binding poses in the putative allosteric pocket that is closest to the orthosteric ligand overlap with the allosteric site predicted by the fragment-based mapping algorithm FTMAP. In spite of most ligand-receptor interactions being the same for the simulated PAM and NAM within this pocket, there are important differences that are being tested experimentally through mutagenesis to assess their functional role.