To generate aerodynamic forces required for flight, two-winged insects (Diptera) move their wings back and forth at high wing-beat frequencies. This results in exceptionally high wing-stroke accelerations, and consequently relatively high acceleration-dependent fluid forces. Quasi-steady fluid force models have reasonable success in relating the generated aerodynamic forces to the instantaneous wing motion kinematics. However, existing approaches model the stroke-rate and stroke-acceleration effects independently from each other, which might be too simplified for capturing the complex unsteady aerodynamics of accelerating wings. Here, we use computational-fluid-dynamics simulations to systematically explore how aerodynamic forces and flow dynamics depend on wing-stroke rate, wing-stroke acceleration and wing-planform geometry. Based on this, we developed and calibrated a novel unsteady aerodynamic force model for insect wings with stroke accelerations. This includes improved versions of the translational-force model and the added-mass force model, and we identify a third novel component generated by the interaction of the two. This term reflects the delay in bound-circulation build-up as the wing accelerates. The physical interpretation of this effect is analogous to the Wagner effect experienced by a wing starting from rest. Here, we show that this effect can be modelled in the context of flapping wings as a stroke-acceleration-dependent correction on the translational-force model. Our revised added-mass model includes a viscous force component, which is relatively small but not negligible. We subsequently applied our new model to realistic wing-beat kinematics of hovering Dipteran insects, in a quasi-steady approach. This revealed that stroke-acceleration-related aerodynamic forces contribute substantially to lift and drag production, particularly for high-frequency flapping mosquito wings.