The combined actions of proteins in networks underlie all fundamental cellular functions. Deeper insights into the dynamics of network composition across species and their functional consequences are crucial to fully understand protein network evolution. Large-scale comparative studies with high phylogenetic resolution are now feasible through the recent rise in available genomic data sets of both model and nonmodel species. Here, we focus on the polarity network, which is universally essential for cell proliferation and studied in great detail in the model organism, Saccharomyces cerevisiae. We examine 42 proteins, directly related to cell polarization, across 298 fungal strains/species to determine the composition of the network and patterns of conservation and diversification. We observe strong protein conservation for a group of 23 core proteins: >95% of all examined strains/species possess at least 14 of these core proteins, albeit in varying compositions, and non of the individual core proteins is 100% conserved. We find high levels of variation in prevalence and sequence identity in the remaining 19 proteins, resulting in distinct lineage-specific compositions of the network in the majority of strains/species. We show that the observed diversification in network composition correlates with lineage, lifestyle, and genetic distance. Yeast, filamentous and basal unicellular fungi, form distinctive groups based on these analyses, with substantial differences to their polarization network. Our study shows that the fungal polarization network is highly dynamic, even between closely related species, and that functional conservation appears to be achieved by varying the specific components of the fungal polarization repertoire.