Pea (Pisum sativum L.) is an important temperate legume crop providing plant-based proteins for food and feed worldwide. Pea yield can be limited by several biotic stresses, among which rust represents a major limiting factor in many temperate and subtropical regions. Some efforts have been made to assess the natural variation in pea resistance to rust, but its efficient exploitation in breeding is limited since the resistance loci identified so far are scarce and their responsible gene(s) unknown. To overcome this knowledge gap, a comprehensive genome-wide association study (GWAS) has been performed on pea rust, caused by Uromyces pisi, to uncover genetic loci associated with resistance. Utilizing a diverse collection of 320 pea accessions, we evaluated phenotypic responses to two rust isolates using both traditional methods and advanced image-based phenotyping. We detected 95 significant trait-marker associations using a set of 26,045 Diversity Arrays Technology-sequencing polymorphic markers. Our in silico analysis identified 62 candidate genes putatively involved in rust resistance, grouped into different functional categories such as gene expression regulation, vesicle trafficking, cell wall biosynthesis, and hormonal signaling. This research highlights the potential of GWAS to identify molecular markers associated with resistance and candidate genes against pea rust, offering new targets for precision breeding. By integrating our findings into current breeding programs, we can facilitate the development of pea varieties with improved resistance to rust, contributing to sustainable agricultural practices and food security. This study sets the stage for future functional genomic analyses and the application of genomic selection approaches to enhance disease resistance in peas.