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The ability to keep a mental record of specific past events, dubbed episodic memory (EM), is key to lifespan adaptation. Nonetheless, the neural mechanisms underlying its typical inter-individual variability remain poorly understood. To address this issue, we tested whether individual differences in EM could be predicted from levels of functional brain re-organization between rest and task modes relevant to the transformation of perceptual information into mental representations (relational processing, meaning extraction, online maintenance versus updating of bound perceptual features). To probe the trait specificity of our model, we included three additional core mental functions, processing speed, abstract reasoning, and cognitive control. Finally, we investigated the extent to which our proposed model reflected genetic versus environmental contributions to EM variability. Hypotheses were tested by applying graph theoretical analysis and structural equation modeling to resting state and task fMRI data from two samples of participants in the Human Connectome Project (Sample 1: N = 338 unrelated individuals; Sample 2: N = 268 monozygotic vs. dizygotic twins [134 same-sex pairs]). Levels of functional brain reorganization between rest and the scrutinized task modes, particularly relational processing and online maintenance of bound perceptual features, contributed substantially to variations in both EM and abstract reasoning (but not in cognitive control or processing speed) among the younger adults in our sample, implying a substantial neurofunctional overlap, at least during this life stage. Similarity in functional organization between rest and each of the scrutinized task modes drew on distinguishable neural resources and showed differential susceptibility to genetic versus environmental influences. Our results suggest that variability on complex traits, such as EM, is supported by neural mechanisms comprising multiple components, each reflecting a distinct pattern of genetic versus environmental contributions and whose relative importance may vary across typical versus psychopathological development.Task-rest similarity in brain connectivity predicts trait episodic memory.The diagnostic tasks require binding and online maintenance of perceptual features.For each task, different brain connections show similarity to rest.Brain connectivity similarity between rest and each task shows differential heritability.The above effects generalize to abstract reasoning, but not other cognitive traits.