Genome size varies by several magnitudes among eukaryotes. Expansion and contraction are primarily driven by transposable element activity, but the underlying processes remain enigmatic due to a lack of historical records tracing these changes. Here, we present the TE Evolution Simulation Suite, or TESS, for versatile simulation of whole-genome sequences with varying transposon dynamics. We analyzed the pangenome of Pucciniomycotina, a subdivision of fungi containing the myrtle rust (Austropuccinia psidii) genome, which drastically expanded to 1018 Mb. Using TESS, we simulated digital replicas of Pucciniomycotina genomes and replicated the genome size evolution of A. psidii driven by LTR retrotransposons.