Intrinsic timescales of activity fluctuations vary hierarchically across the brain. This variation reflects a broad gradient of functional specialization in information storage and processing, with integrative association areas displaying slower timescales that are thought to reflect longer temporal processing windows. The organization of timescales is associated with cognitive function, distinctive between individuals, and disrupted in disease, but we do not yet understand how the temporal properties of activity dynamics are shaped by the brain’s underlying structural connectivity network. Using resting-state fMRI and diffusion MRI data from 100 healthy individuals from the Human Connectome Project, here we show that the timescale of resting-state fMRI dynamics increases with structural connectivity strength, matching recent results in the mouse brain. Our results hold at the level of individuals, are robust to parcellation schemes, and are conserved across a range of different timescale- related statistics. We establish a comprehensive BOLD dynamical signature of structural connectivity strength by comparing over 6,000 time series features, highlighting a range of new temporal features for characterizing BOLD dynamics, including measures of stationarity and symbolic motif frequencies. Our findings indicate a conserved property of mouse and human brain organization in which a brain region’s spontaneous activity fluctuations are closely related to their surrounding structural scaffold.