The prediction of structural vibrations induced by high-speed trains is crucial for designing bridge structures, as well as for the assessment of the dynamic compatibility between bridges and rolling stock in large railway networks. The computational effort involved in such dynamic compatibility checks is also large. However, obtaining an accurate prediction of the dynamic response is challenging due to numerous uncertain factors still under research. Interaction phenomena like vehicle–bridge (VBI), soil–structure (SSI), and track–bridge (TBI) interactions are crucial but complex to model, given the multitude of input parameters and the computational cost required. Therefore, the choice of a modelling approach for simulating the dynamic response of a train crossing a bridge will depend on the focus of analysis. For the purpose of sensitivity analyses – typical in early design stages –, compatibility checks (screenings), and also in non-deterministic analyses, computational cost becomes crucial. Consequently, for practical purposes interaction mechanisms are often simulated by means of simplified and conservative approaches, usually aligned with some design code recommendations. Moreover, traditional physical models, where the problem is idealised as a beam traversed by constant moving loads (travelling load model, TLM), have been commonly employed for such purposes. However, they neglect the load distributive effect of the track on the vehicle axle loads, which has proven to be relevant and beneficial, especially for short bridge spans. The main purpose of this work is thus to investigate the influence of the load spreading effect exerted by the ballasted track on the displacement and acceleration response of single-track, simply-supported (S-S) railway bridges of short-to-medium span lengths under operating conditions, since these structures are prone to experience inadmissible vibration levels under more demanding traffic conditions. A comprehensive analysis of several simplified approaches proposed by regulations and researchers is performed, plus a subsequent comparison vs. a finite element (FE) strategy to consider TBI in a refined manner. Conclusions about the adequacy of the simplified approaches are provided, along with a new data-driven formula for the prediction of the vertical displacement response in resonant conditions, that can be exploited to reduce significantly the computational effort.