Resting-state EEG reflects intrinsic brain activity and its alteration represents changes in cognition that are related to neuropathology. Thereby, it provides a way of revealing the neurocognitive mechanisms underpinning chronic substance use. In addition, it is documented that some neurocognitive functions can recover following sustained abstinence. We present a systematic review to synthesize how chronic substance use is associated with resting-state EEG alterations and whether these spontaneously recover from abstinence. A literature search in Medline, PsycINFO, Embase, CINAHL, Web of Science, and Scopus resulted in 4088 articles, of which 57 were included for evaluation. It covered the substance of alcohol (18), tobacco (14), cannabis (8), cocaine (6), opioids (4), methamphetamine (4), and ecstasy (4). EEG analysis methods included spectral power, functional connectivity, and network analyses. It was found that long-term substance use with or without substance use disorder diagnosis was associated with broad intrinsic neural activity alterations, which were usually expressed as neural hyperactivation and decreased neural communication between brain regions. Some studies found the use of alcohol, tobacco, cocaine, cannabis, and methamphetamine was positively correlated with these changes. These alterations can partly recover from abstinence, which differed between drugs and may reflect their neurotoxic degree. Moderating factors that may explain results inconsistency are discussed. In sum, resting-state EEG may act as a potential biomarker of neurotoxic effects of chronic substance use. Recovery effects awaits replication in larger samples with prolonged abstinence. Balanced sex ratio, enlarged sample size, advanced EEG analysis methods, and transparent reporting are recommended for future studies.