The roles and positive impacts of business incubators, including virtual ones, in promoting entrepreneurship and innovation in multiple industries, and their consequent contributions to fostering sustainable economic growth and social development, have been highly advocated in the extant literature. Nonetheless, several authors highlight the urgent need to further carry out research concerning these structures’ operation models by involving end users, since knowledge related to this phenomenon remains scant. This study sets out to convey the third phase of a broader research and development project following a design science research methodology. Ultimately, this contributes to the field by proposing a new virtual business incubator model with immediate practical applicability. This model was cocreated and validated with 23 incubator managers and startup founders from 15 business incubation centers during focus group sessions and organized into 8 dimensions concluded as fundamental in future digital incubation programs. Moreover, this study offers knowledgeable guidelines to support academics, practitioners, organization managers, or other professionals interested in building and running virtual business incubators. The main strengths and weaknesses of the proposed model are also highlighted, and several recommendations are provided to surpass the expected challenging stages of its implementation.