The lateral and capsular divisions of the central amygdala (CeLC) is a key region involved in the processing of emotional-affective dimensions of pain. In the spino-parabrachio-amygdaloid pain pathway, the CeLC receives nociceptive information from calcitonin gene-related peptide (CGRP) neurons in the parabrachial nucleus. Recent evidence indicates that glutamate delta receptor 1 (GluD1) regulates this projection in mice. GluD1 is an atypical ionotropic glutamate receptor that largely functions as a synaptogenic molecule involved in the formation and maintenance of synapses. Despite its strong cellular expression, little is known about the subsynaptic localization of GluD1 and its potential interaction with CGRP terminals in CeLC neurons. To address this issue, we used single and double immuno-electron microscopy techniques in rodents and monkeys. In both species, CGRP-positive (CGRP+) terminals formed symmetric and asymmetric synapses with dendrites, symmetric synapses with soma, and less commonly, asymmetric synapses with spines. Approximately 80% of CGRP+ terminals forming clear symmetric synapses expressed vGluT2 immunoreactivity and none were immunoreactive for GABA, confirming the glutamatergic nature of this projection and suggesting that some PB-CGRP terminals may modulate transmission to the CeLC in a peptidergic manner. GluD1 was expressed in the core of symmetric axo-dendritic and axo-somatic synapses and peri-synaptic to asymmetric synapses. These findings show that the ascending CGRP+PB-CeLC projection mediates its effects through a heterogenous population of terminals that display strong synaptic relationships with GluD1 in both mice and monkeys.