Studies have shown altered task-based brain functioning as a result of cannabis use. To date, however, whether similar alterations in baseline resting state and functional organization of neural activity are observable in cannabis users remains unknown. We characterized global resting state cortical activations and functional connectivity via electroencephalography (EEG) in cannabis users and related these activations to measures of cannabis use. Resting state EEG in the eyes closed condition was collected from age- and sex-matched cannabis users (N = 17; 6 females; mean age = 30.9 ± 7.4 years) and non-using controls (N = 21; 9 females; mean age = 33.1 ± 11.6 years). Power spectral density and spectral coherence were computed to determine differences in cortical activations and connectivity between the two groups in the delta (1–4Hz), theta (4–7 Hz), alpha (8–12 Hz), beta (13–30 Hz), and gamma (31–50 Hz) frequency bands. Cannabis users exhibited decreased delta and increased theta, beta, and gamma power compared to controls, suggesting increased cortical activation in resting state and a disinhibition of inhibitory functions that may interrupt cognitive processes. Cannabis users also exhibited increased interhemispheric and intrahemispheric coherence relative to controls, reduced mean network degree, and increased clustering coefficient in specific regions and frequencies. This increased cortical activity may indicate a loss of neural refinement and efficiency that may indicate a “noisy” brain. Lastly, measures related to cannabis use were correlated with spectral power and functional connectivity measures, indicating that specific electrophysiological signals are associated with cannabis use. These results suggest that there are differences in cortical activity and connectivity between cannabis users and non-using controls in the resting state that may be related to putative cognitive impairments and can inform effectiveness of intervention programs.