Exposure to a real or perceived threat elicits multiple behavioral and physiological consequences collectively known as the stress response. One consequence is the activation of the hypothalamic pituitary adrenal (HPA) axis, where release of corticotropin-releasing hormone (CRH) from the paraventricular nucleus of the hypothalamus (PVN) results in elevated circulating corticosterone (CORT). CRH neurons in the PVN (CRHPVN) are also implicated in several stress-induced behaviors, such as grooming. Although the physiological processes involved in responding to a stressor have been relatively well elucidated, less attention has been paid to what gates this response in the absence of a threat. The endocannabinoid (eCB) is involved in many arms of the stress response. However, current research paints a superficial picture of how eCB signaling provides tonic and phasic regulation of the stress response. This thesis utilizes cellular, neuroendocrine and behavioral measures together to capture a broad picture of how tonic and phasic eCB signaling regulates the stress response. Aim1: Systemic administration of a CB1 receptor antagonist/inverse agonist (AM251), neutral antagonist (NESS0327) and AEA synthesis inhibitor (LEI401) all elevated cellular activity in the PVN, circulating CORT and homecage grooming behaviors, suggesting a role for AEA as the tonic regulator of the stress response. Intra-PVN AM251 administration increased stress-like grooming and circulating CORT, providing evidence for local tonic eCB signaling in gating the stress response in the absence of a stressor. Aim2: Pharmacological blockade of 2-AG degradation, but not AEA, with JZL184 accelerated the behavioral recovery following a footshock stressor, while elevating c-fos expression in the PVN and circulating CORT. Intra-PVN JZL184 infusions recapitulated the behavioral effects of systemic administrations while also blunting stress-induced increases in circulating CORT. Systemic JZL184 administrations had a biphasic influence on CRHPVN neuron activity, amplifying population activity in a threatening environment but accelerating CRHPVN recovery following return to homecage. Overall, these data identify AEA as a tonic gatekeeper of the stress response in the absence of a threat and 2-AG as providing a phasic response to a stressful stimulus, shutting the stress response down during recovery. These data provide the groundwork necessary to develop therapies targeting the treatment of stress-related disorders.