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Cannabis Use Disorder (CUD) affects ~ 50 million individuals globally. CUD has been associated with adverse psychosocial outcomes, including affective flattening, apathy, and anhedonia, which prominent neuroscientific theories ascribe (in part) to altered integrity in brain reward pathways. Yet, emerging evidence from functional neuroimaging (fMRI) is mixed. We examined the activity in key regions-of-interest (ROIs) of the reward neurocircuitry in moderate-to-severe CUD vs. controls, and associations with cannabis use patterns in addition to Apathy Evaluation Scale scores. Brain reward function was examined in 57 people with moderate-to-severe CUD and 35 age and sex-matched controls using the Monetary Incentive Delay fMRI task. We compared brain function between groups, adjusting for age and sex, using exploratory whole-brain and hypothesis-driven ROI analyses in the ventral striatum, dorsal caudate, putamen, insula, cingulate, and orbitofrontal cortices. ROI analyses showed greater activity in the CUD vs. control group in bilateral insula and right putamen when receiving monetary wins vs. receiving neutral wins (i.e., outcomes with no monetary gain). The ROI analysis also showed greater activity in the CUD vs. controls in the right putamen when receiving monetary wins vs. receiving missed monetary wins. There were no other significant effects for the other ROIs, the whole-brain analyses, or brain-behaviour correlations. Overall, people with CUD showed altered activity in key brain reward regions during the receipt phase of rewards, compared to controls.