The timing of activity across brain regions can be described by its phases for oscillatory processes, and is of crucial importance for brain functioning. The structure of the brain constrains its dynamics through the delays due to propagation and the strengths of the white matter tracts. We use self-sustained delay-coupled, non-isochronous, nonlinearly damped and chaotic oscillators to study how spatio-temporal organization of the brain governs phase lags between the coherent activity of its regions. In silico results for the brain network model demonstrate a robust switching from in- to anti-phase synchronization by increasing the frequency, with a consistent lagging of the stronger connected regions. Relative phases are well predicted by an earlier analysis of Kuramoto oscillators, confirming the spatial heterogeneity of time delays as a crucial mechanism in shaping the functional brain architecture. Increased frequency and coupling are also shown to distort the oscillators by decreasing their amplitude, and stronger regions have lower, but more synchronized activity. These results indicate specific features in the phase relationships within the brain that need to hold for a wide range of local oscillatory dynamics, given that the time delays of the connectome are proportional to the lengths of the structural pathways. This article is part of the theme issue ‘Nonlinear dynamics of delay systems’.