Background: Alzheimer’s disease (AD) includes progressive symptoms spread along a continuum of preclinical and clinical stages. Although numerous studies uncovered the neuro-cognitive changes of AD, very little is known on the natural history of brain lesions and modifications of brain networks in elderly cognitively-healthy memory complainers at risk of AD for carrying pathophysiological biomarkers (amyloidopathy and tauopathy). Objective: We analyzed resting-state electroencephalography (EEG) of 318 cognitively-healthy subjective memory complainers from the INSIGHT-preAD cohort at the time of their first visit (M0) and two-years later (M24). Methods: Using 18F-florbetapir PET-scanner, subjects were stratified between amyloid negative (A–; n = 230) and positive (A+; n = 88) groups. Differences between A+ and A–were estimated at source-level in each band-power of the EEG spectrum. Results: At M0, we found an increase of theta power in the mid-frontal cortex in A+ compared to A–. No significant association was found between mid-frontal theta and the individuals’ cognitive performance. At M24, theta power increased in A+ relative to A–individuals in the posterior cingulate cortex and the pre-cuneus. Alpha band revealed a peculiar decremental trend in posterior brain regions in the A+ relative to the A–group only at M24. Theta power increase over the mid-frontal and mid-posterior cortices suggests an hypoactivation of the default-mode network in the A+ individuals and a non-linear longitudinal progression at M24. Conclusion: We provide the first source-level longitudinal evidence on the impact of brain amyloidosis on the EEG dynamics of a large-scale, monocentric cohort of elderly individuals at-risk for AD.