The growing world population in combination with the anticipated effects of climate change pressures food security. Plants display an impressive arsenal of cellular mechanisms for resilience to adverse environmental conditions and we rely on those mechanism for stable food production. The elucidation of the molecular basis of the mechanisms plants use to achieve resilience promises knowledge-based approaches to enhance food security. DNA sequence polymorphisms can reveal genomic regions that are linked to beneficial traits of plants. However, our ability to interpret how a given DNA sequence polymorphism confers a fitness advantage on the molecular level remains often poor. A key factor is that these polymorphisms largely localize to the enigmatic non-coding genome. Here, we review the functional impact of sequence variations in the non-coding genome on plant biology in the context of crop breeding and agricultural traits. We focus our review on examples of non-coding with particularly convincing functional support. Our survey combines findings that are consistent with the view that that the non-coding genome contributes to cellular mechanisms assisting many plant traits. Understanding how DNA sequence polymorphisms in the non-coding genome shape plant traits on the molecular level offers a largely unexplored reservoir of solutions to address future challenges in plant growth and resilience.