Fungal vegetative incompatibility is a key barrier for exploring hypovirulence-associated mycoviruses to control plant fungal diseases. A novel mycoreovirus, Sclerotinia sclerotiorum mycoreovirus 4 (SsMYRV-4), which was originally isolated from strain SX10, confers hypovirulence on the plant pathogenic fungus S. sclerotiorum. The genome of SsMYRV-4 consists of twelve linear dsRNA segments (S1-S12), and is closely related to Rosellinia necatrix mycoreovirus 3. Virus-like particles (VLPs) are approximately 60~70 nm in diameter, and localize near the nuclear membrane of S. sclerotiorum. Interestingly, SsMYRV-4 could inhibit cellular production of reactive oxygen species (ROS) and down-regulate expression of two ROS-associated genes, and finally attenuate host vegetative incompatibility reaction via termination of the incompatible programmed cell death reaction. Mycovirus transmission efficiency was significantly increased among vegetatively incompatible groups in the presence of SsMYRV-4 infection donor strains. In addition, SsMYRV-4 benefits for S. sclerotiorum tolerance to diverse stresses. Our findings suggested that hypovirulence-associated mycoviruses could be horizontally transmitted between vegetatively incompatible groups via creation of a bridge strain infected with SsMYRV-4. These discoveries provide new insights into mycovirus ecological activities as well as presenting a new potential strategy of mycovirus application for biological control under natural conditions.