The semantic integration between gesture and speech (GSI) is mediated by the left posterior temporal sulcus/middle temporal gyrus (pSTS/MTG) and the left inferior frontal gyrus (IFG). Evidence from electroencephalography (EEG) suggests that oscillations in the alpha and beta bands may support processes at different stages of GSI. In the present study, we investigated the relationship between electrophysiological oscillations and blood-oxygen-level-dependent (BOLD) activity during GSI. In a simultaneous EEG-fMRI study, German participants (n = 19) were presented with videos of an actor either performing meaningful gestures in the context of a comprehensible German (GG) or incomprehensible Russian sentence (GR), or just speaking a German sentence (SG). EEG results revealed reduced alpha and beta power for the GG vs. SG conditions, while fMRI analyses showed BOLD increase in the left pSTS/MTG for GG > GR ∩ GG > SG. In time-window-based EEG-informed fMRI analyses, we further found a positive correlation between single-trial alpha power and BOLD signal in the left pSTS/MTG, the left IFG, and several sub-cortical regions. Moreover, the alpha-pSTS/MTG correlation was observed in an earlier time window in comparison to the alpha-IFG correlation, thus supporting a two-stage processing model of GSI. Our study shows that EEG-informed fMRI implies multiple roles of alpha oscillations during GSI, and that the method is a best candidate for multidimensional investigations on complex cognitive functions such as GSI.