Development and virulence of the vascular plant pathogen Verticillium dahliae are connected and depend on a complex interplay between the unfolded protein response, a Ham5 independent pheromone MAP kinase module and formation of precursors for oxylipin signal molecules. Genes coding for the unfolded protein response regulator Hac1, the Ham5 MAPK scaffold protein, and the oleate Δ12-fatty acid desaturase Ode1 were deleted and their functions in growth, differentiation, and virulence on plants were studied using genetic, cell biology, and plant infection experiments. The unfolded protein response transcription factor Hac1 is required for initial root colonization, fungal conidiation and propagation inside the host and is essential for resting structure formation. Microsclerotia development, growth and virulence require the pheromone response MAPK pathway, but without the Ham5 scaffold function. Single ER-associated enzymes for linoleic acid production make important contributions to fungal growth but have only a minor impact on the pathogenicity of V. dahliae. Fungal growth, sporulation, dormant structure formation and plant infection require a network of the Hac1-regulated unfolded protein response, a scaffold-independent pheromone response MAPK pathway and formation of precursors for signalling. This network includes interesting targets for disease management of the vascular pathogen V. dahliae.