Plants balance the allocation of resources between growth and defence to optimize fitness in a competitive environment. Perception of neighbour-detection cues, such as a low ratio of red to far-red (R:FR) radiation, activates a suite of shade-avoidance responses that include stem elongation and upward leaf movement, whilst simultaneously downregulating defence. This downregulation is hypothesized to benefit the plant either by mediating the growth-defence balance in favour of growth in high plant densities or, alternatively, by mediating defence of individual leaves such that those most photosynthetically productive are best protected. To test these hypotheses, we used a 3D functional–structural plant model of Brassica nigra that mechanistically simulates the interactions between plant architecture, herbivory, and the light environment. Our results show that plant-level defence expression is a strong determinant of plant fitness and that leaf-level defence mediation by R:FR can provide a fitness benefit in high densities. However, optimal plant-level defence expression does not decrease monotonically with plant density, indicating that R:FR mediation of defence alone is not enough to optimize defence between densities. Therefore, assessing the ecological significance of R:FR-mediated defence is paramount to better understand the evolution of this physiological linkage and its implications for crop breeding.