Somatic cell fusion contributes to colony establishment, development, and long-term fitness in many filamentous ascomycete fungi. Fusion occurs at multiple developmental stages, from spore germination to mature hyphal networks, and is essential for mycelial integration, resource allocation, and developmental plasticity. Research over the past two decades, largely based on Neurospora crassa, has revealed that fungal cell–cell fusion relies involves an unusual “cellular dialog” signaling mechanism, in which interacting cells alternate between sending and receiving signals. This mechanism appears to be highly conserved across ascomycete fungi and even facilitates interspecies interactions. At the same time, stringent self/nonself recognition systems act downstream of communication to restrict fusion to genetically compatible partners. These allorecognition checkpoints, mediated by diverse genetic systems highlight the evolutionary balance between the benefits of cooperation and the risks of genetic conflict or parasitism. Together, these findings reveal a complex interplay between conserved molecular mechanisms of communication and highly diverse, lineage-specific recognition barriers. In this chapter, we summarize the types and functions of somatic fusion, outline the molecular basis of cell–cell communication and membrane merger, and discuss the checkpoints that determine interaction specificity.