Filamentous plant pathogens pose a severe threat to food security. Current estimates suggest up to 23% yield losses to pre- and post-harvest diseases and these losses are projected to increase due to climate change (Singh et al. 2023; Chaloner et al. 2021; Stukenbrock and Gurr 2023; Fisher et al. 2012; Steinberg and Gurr 2020). Understanding how filamentous plant pathogens emerge, spread and adapt to their hosts and new environmental niches is crucial to address their devastating impact on global agriculture. Over the past two decades, genomics has emerged as a central technology to advance our understanding of the population dynamics and coevolution of filamentous plant pathogens. The first genome of a filamentous plant pathogen, the blast fungus Magnaporthe oryzae, was sequenced 20 years ago. Since then, plant pathogen genomics has not only provided a deep understanding of the genomic makeup of plant pathogen populations, but has emerged as a fundamental technology for gene discovery, disease diagnostics, and has accelerated molecular biology. In merely two decades, we have witnessed several revolutions in the field, including the first reference genomes of many filamentous plant pathogens, population scale genomics of thousands of individuals, long-read and chromosome conformation sequencing for highly continuous assemblies and recent intersections of genomics and structural biology. Here, we commemorate the 20th anniversary by presenting important technological advances (Fig. 1) and lessons we learned from the past two decades of filamentous plant pathogen genomics, with a focus on cereal diseases.