Background. The global increase in lenient cannabis policy has been paralleled by reduced harm perception, which has been associated with cannabis use initiation and persistent use. However, it is unclear how cultural attitudes towards cannabis use might affect the brain processes underlying cannabis use. Methods. Resting state functional connectivity (RSFC) within and between the executive control network, salience network, and default mode network was assessed in 110 near-daily dependent cannabis users and 79 controls from The Netherlands and Texas, USA. Participants completed a questionnaire assessing the perceived benefits and harms of cannabis use from their personal, friends-family’s and country-state’s perspective and reported on their cannabis use (gram/week), DSM-5 cannabis use disorder (CUD) symptoms, and cannabis related problems. Results. RSFC within the dorsal salience network was lower in cannabis users than controls and was negatively associated with cannabis use in the cannabis group. Cultural attitudes – from personal, friends-family’s and country-state’s perspectives – moderated the associations of cannabis use, CUD symptoms, and cannabis use related problems with RSFC within the salience, executive control, and default mode networks. No group differences in between-network RSFC were observed, but personal perceived benefits and country-state perceived harms moderated the association between CUD symptoms and RSFC between the dorsal and ventral default mode network. Conclusions. This study highlights the importance of considering individual differences in the perceived harms and benefits of cannabis use as a factor in the associations between brain functioning and cannabis use, CUD symptoms, and cannabis use related problems.