The term functional connectivity is used to describe which parts of the brain work together on a process, and might aid the understanding of how the processing systems in the human brain are fundamentally organised. The default mode network (DMN) is a constellation of cortical structures that has shown remarkable reliability as a resting-state network(RSN). It has often been referred to as a task-negative network, because it typically exhibits amplified activation patterns during rest. Numerous studies have documented DMN alterationsin various clinical conditions, including mild cognitive impairment and Alzheimer’s disease. However, little is known about the impact of normal aging on this network. The present study investigates age–differences in DMN functional connectivity and further, whether the effects of age are modulated by the allelic variation of the alipoprotein E-gene, APOE. Based on current theories of cognitive aging and the few existing previous studies on restingstate patterns and APOE, we have two hypotheses: 1) an elevated co-activation in the DMN with increasing age, and 2) different effects for ε4-carriers compared to non-carriers in the MTL structures, including the hippocampus. We tested these hypotheses on resting-state functional magnetic resonance imaging (fMRI) data from 182 healthy participants aged 20-78 years, including 63 carriers of the ε4-allele. Using a combination of independent component analysis (ICA) and dual-regression, we document regionally specific escalations in DMN synchronicity with increased age, especially in frontal brain areas. Additionally, we observed a moderate negative effect of the ε4-allele in the posterior cingulate cortex (PCC) of the posterior parts of the DMN, indicating lower co-activity in carriers compared to non-carriers in areas spanning core parts of the DMN. These findings are discussed in light of theories of cognitive aging, and we argue that the amplified DMN functional connectivity with age is indicative ofan age-related decrease in neural differentiation manifested as decreased decoupling between task-negative and task-positive brain networks during rest.