Abstract Understanding the relationship between structural connectivity (SC) and functional connectivity (FC) of the human brain is an important goal of neuroscience. Highly detailed mathematical models of neural masses exist that can simulate the interactions between functional activity and structural wiring. These models are often complex and require intensive computation. Most importantly, they do not provide a direct or intuitive interpretation of this structure–function relationship. In this study, we employ the emerging concepts of spectral graph theory to obtain this mapping in terms of graph harmonics, which are eigenvectors of the structural graph’s Laplacian matrix. In order to imbue these harmonics with biophysical underpinnings, we leverage recent advances in parsimonious spectral graph modeling (SGM) of brain activity. Here, we show that such a model can indeed be cast in terms of graph harmonics, and can provide a closed-form prediction of FC in an arbitrary frequency band. The model requires only three global, spatially invariant parameters, yet is capable of generating rich FC patterns in different frequency bands. Only a few harmonics are sufficient to reproduce realistic FC patterns. We applied the method to predict FC obtained from pairwise magnitude coherence of source-reconstructed resting-state magnetoencephalography (MEG) recordings of 36 healthy subjects. To enable efficient model inference, we adopted a deep neural network-based Bayesian procedure called simulation-based inference. Using this tool, we were able to speedily infer not only the single most likely model parameters, but also their full posterior distributions. We also implemented several other benchmark methods relating SC to FC, including graph diffusion and coupled neural mass models. The present method was shown to give the best performance overall. Notably, we discovered that a single biophysical parameterization is capable of fitting FCs from all relevant frequency bands simultaneously, an aspect that did not receive adequate attention in prior computational studies.