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Supergenes are tightly linked sets of loci that are inherited together and control complex phenotypes. While classical supergenes—governing traits such as wing patterns in Heliconius butterflies or heterostyly in Primula —have been studied since the Modern Synthesis, we still understand very little about how they evolve and persist in nature. The genetic architecture of supergenes is a critical factor affecting their evolutionary fate, as it can change key parameters such as recombination rate and effective population size, potentially redirecting molecular evolution of the supergene in addition to the surrounding genomic region. To understand supergene evolution, we must link genomic architecture with evolutionary patterns and processes. This is now becoming possible with recent advances in sequencing technology and powerful forward computer simulations. The present theme issue brings together theoretical and empirical papers, as well as opinion and synthesis papers, which showcase the architectural diversity of supergenes and connect this to critical processes in supergene evolution, such as polymorphism maintenance and mutation accumulation. Here, we summarize those insights to highlight new ideas and methods that illuminate the path forward for the study of supergenes in nature. This article is part of the theme issue ‘Genomic architecture of supergenes: causes and evolutionary consequences’.