SummaryResearch on obligate biotrophic plant parasites, which reproduce only on living hosts, has revealed a broad diversity of filamentous microbes that have independently acquired complex morphological structures, such as haustoria. Genome studies have also demonstrated a concerted loss of genes for metabolism and lytic enzymes, and gain of diversity of genes coding for effectors involved in host defense suppression. So far, these traits converge in all known obligate biotrophic parasites, but unexpected genome plasticity remains. This plasticity is manifested as transposable element (TE)‐driven increases in genome size, observed to be associated with the diversification of virulence genes under selection pressure. Genome expansion could result from the governing of the pathogen response to ecological selection pressures, such as host or nutrient availability, or to microbial interactions, such as competition, hyperparasitism and beneficial cooperations. Expansion is balanced by alternating sexual and asexual cycles, as well as selfing and outcrossing, which operate to control transposon activity in populations. In turn, the prevalence of these balancing mechanisms seems to be correlated with external biotic factors, suggesting a complex, interconnected evolutionary network in host–pathogen–microbe interactions. Therefore, the next phase of obligate biotrophic pathogen research will need to uncover how this network, including multitrophic interactions, shapes the evolution and diversity of pathogens. Contents Summary 1207 I. Introduction 1208 II. Mechanisms of convergent evolution in obligate plant parasitism 1209 III. Obligate biotrophy does not constrain genome size 1211 IV. Sexual and asexual cycles balance genome size variation 1217 V. Haploid or diploid: which phase dominates? 1218 VI. Comparative genomics and effector evolution: what have we learned? 1219 VII. Obligate biotrophy and the microbiome 1221 VIII. Conclusions and research needs: biotrophic pathogens are a dynamic threat to food security and unpredictable without the understanding of their evolutionary and ecological networks 1224 Acknowledgements 1224 References 1224