Despite extensive research, pro-angiogenic drugs have failed to translate clinically, and therapeutic angiogenesis, which has potential in the treatment of various cardiovascular diseases, remains a major challenge. Physiologically, angiogenesis - the process of blood-vessel growth from existing vasculature - is regulated by a complex interplay of biophysical and biochemical cues from the extracellular matrix (ECM), angiogenic factors and multiple cell types. The ECM can be regarded as the natural 3D material that regulates angiogenesis. Here, we leverage knowledge of ECM properties to derive design rules for engineering pro-angiogenic materials. We propose that pro-angiogenic materials should be biomimetic, incorporate angiogenic factors and mimic cooperative interactions between growth factors and the ECM. We highlight examples of material designs that demonstrate these principles and considerations for designing better angiogenic materials.