The basolateral amygdala (BLA) is essential for assigning positive or negative valence to sensory stimuli in an animal’s environment. Noxious stimuli that cause pain are encoded by an ensemble of nociceptive BLA projection neurons (BLAnoci ensemble). The BLAnoci ensemble is responsive to noxious stimuli across sensory modalities and not responsive to non-noxious aversive nor appetitive stimuli. However, the role of the BLAnoci ensemble in mediating behavior changes, the molecular signatures, and the downstream targets distinguishing this ensemble remain poorly understood. Here, we show that the same BLAnoci ensemble neurons are stable across pain states and are required for both acute and chronic neuropathic pain behavior, though are not sufficient to drive nociceptive behaviors. Using single nucleus RNA-sequencing, we characterized the effect of acute and chronic pain on the BLA for the first time and identified single nuclei that are more responsive to noxious stimuli. We identified enrichment for genes with known functions in axonal and synaptic organization and pain perception. We thus examined the brain-wide targets of the BLAnoci ensemble in affective pain brain regions. We uncovered a previously undescribed nociceptive hotspot of the nucleus accumbens shell (NAcSh). The NAcShnoci ensemble mirrors the stability and specificity of the BLAnoci ensemble and displays similar calcium dynamics as the BLAnoci ensemble. Notably, BLAnoci ensemble axons transmit acute and neuropathic nociceptive information to the NAcSh, highlighting this nociceptive amygdala-striatal circuit as a unique pathway for affective-motivational responses across pain states. Finally, we show that inhibition of the NAcShnoci ensemble alone is not sufficient to reduce nociceptive responses or pain-induced negative affective behavior, suggesting that the upstream signal of the BLAnoci ensemble may be transmitted to other brain regions that are driving these responses. In all, we describe a vital node of the affective pain pathway that seems particularly important for transmitting information about the development of chronic pain.