Aging is accompanied by changes in brain architecture that alter the lateralization of functional networks. In this study, we examined how hemispheric specialization changes across the adult lifespan by analyzing resting-state fMRI and structural MRI data from 728 typical adults aged 18 to 88 years. Using the Language-and-Memory Network atlas, we quantified regional asymmetries in functional connectivity along the cortex's principal gradient, and normalized regional volumes across 37 bilateral regions. We identified two distinct age-related asymmetry trajectories: one pattern revealed a bilateralization of language-dominant regions, while the other showed increasing leftward specialization in multimodal regions associated with memory and language. These opposing patterns emerged around midlife and were linked to performance in language production tasks. By integrating connectivity gradients, structural asymmetries, and behavioral data, our findings provide new evidence for a dual mechanism reshaping functional brain lateralization with age and demonstrate the utility of resting-state metrics in tracking these shifts.