Drugs such as morphine target opioid receptors to provide effective analgesia. These effects are mostly mediated through µ-opioid receptor (MOR) and are accompanied by many adverse side effects. The δ-opioid receptor (DOR) is emerging as a potential therapeutic target for pain relief that may result in fewer such side effects, particularly due to suggested expression of DOR in peripheral nociceptors which opens an avenue for peripherally active DOR-targeting pharmaceutics. Moreover, accumulating evidence suggests that following inflammation, the analgesic effects of DOR agonists are increased. However, the extent of expression of functional DORs in the plasma membrane of peripheral nociceptors and the mechanisms of regulation of DOR plasma membrane abundance remains highly controversial. In this study we used patch-clamp recordings and total internal reflection fluorescence (TIRF) microscopy to study functional expression of DOR in sensory neurons from rat trigeminal ganglia (TG) and the role of inflammatory mediator bradykinin (BK) in the control of the pool size of DOR-positive neurons in TG. As a readout of functional activity of DOR we used the inhibition of voltage-gated calcium channels (VGCC) by DOR agonists. Using patch-clamp, we found that DOR agonist [D-Ala2, D-Leu5] – Enkephalin (DADLE, 200 nM) inhibited VGCC by 23.6 ± 5.86% (S.E.M.) in a DOR specific, reversible and PTX sensitive manner, in 36% of cultured TG neurons (8/22). Real-time TIRF microscopy revealed that BK treatment caused robust trafficking of DOR to the plasma membrane (5/8). Interestingly, pre-treatment with BK resulted in a large increase in the population of DOR-positive neurons, but did not affect the degree of VGCC inhibition by DADLE. Thus, in BK treated TG neuron cultures, 66% of the population responded to DADLE (10/15) with inhibition that amounted to 21.3 ± 5.14% (S.E.M.) of macroscopic VGCC current (n=10). Ca2+ imaging experiments revealed that 80% of cultured TG neurons respond to BK with robust Ca2+ signals (n=44), thus, our data suggest that an overwhelming majority of a large BK-responsive population of TG neurons have a potential to become DOR-positive upon inflammation. Our study re-establishes the therapeutic potential of peripheral DOR in treatment of inflammatory pain.