Functional brain aging is often characterized by differences between people of different ages, although aging unfolds within individuals. This distinction is especially important for functional connectivity, where the direction of covariance change may evolve across adulthood. We introduce a Bayesian longitudinal covariance-operator framework that models each visit covariance as a latent positive-definite state informed by repeated resting-state fMRI runs. The approach calibrates run-level information for temporal dependence and replicate variability, separates within-person aging from between-person age differences, and uses an adaptive tangent representation to learn the low-dimensional structure of longitudinal change without relying on pooled covariance variation. The longitudinal operator varies smoothly in magnitude and orientation with age, while exact Fréchet derivatives translate the fitted trajectory to the covariance scale. This framework allows us to examine how brain covariance organization changes within individuals, whether longitudinal aging follows the population age gradient, and which functional systems contribute to their divergence. In the Dallas Lifespan Brain Study, within-person covariance aging differs substantially from the cross-sectional age gradient through early and middle adulthood, with the discrepancy diminishing later in life. Covariance reorganization is strongest around midlife, and the longitudinal signal is concentrated in a few coordinated directions, with most off-diagonal change occurring between functional systems. These findings demonstrate that population-level signatures of brain aging do not necessarily reflect individual aging trajectories and highlight the importance of modeling longitudinal covariance change directly.

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