It remains a puzzling issue why and how the organs in plants living in the same natural environment evolve into a wide variety of geometric architecture. In this work, we explore, through a combination of experimental and numerical methods, the biomechanical morphogenesis of the leaves and stalks of representative emergent plants, which can stand upright and survive in harsh water environments. An interdisciplinary topology optimization method is developed here by integrating both mechanical performance and biological constraint into the bi-directional evolutionary structural optimization technique. The experimental and numerical results reveal that, through natural selection over many million years, these leaves and stalks have been optimized into distinctly different cross-sectional shapes and aerenchyma tissues with intriguing anatomic patterns and improved load-bearing performance. The internal aerenchyma is an optimal compromise between the mechanical performance and functional demands such as air exchange and nutrient transmission. We find that the optimal distribution of the internal material depends on multiple biomechanical factors such as the cross-sectional geometry, hierarchical structures, boundary condition, biological constraint, and material property. This work provides an in-depth understanding of the property–structure–performance–function interrelations of biological materials. The proposed topology optimization method and the presented biophysical insights hold promise for designing highly efficient and advanced structures (e.g., airplane wings and turbine blades) and analyzing other biological materials (e.g., bones, horns, and beaks).