Fungi and oomycetes are filamentous microorganisms that include a diversity of highly developed pathogens of plants. These are sophisticated modulators of plant processes that secrete an arsenal of effector proteins to target multiple host cell compartments and enable parasitic infection. Genome sequencing revealed complex catalogues of effectors of filamentous pathogens, with some species harboring hundreds of effector genes. Although a large fraction of these effector genes encode secreted proteins with weak or no sequence similarity to known proteins, structural studies have revealed unexpected similarities amid the diversity. This article reviews progress in our understanding of effector structure and function in light of these new insights. We conclude that there is emerging evidence for multiple pathways of evolution of effectors of filamentous plant pathogens but that some families have probably expanded from a common ancestor by duplication and diversification. Conserved folds, such as the oomycete WY and the fungal MAX domains, are not predictive of the precise function of the effectors but serve as a chassis to support protein structural integrity while providing enough plasticity for the effectors to bind different host proteins and evolve unrelated activities inside host cells. Further effector evolution and diversification arise via short linear motifs, domain integration and duplications, and oligomerization.