No previous organization has managed to execute such a widespread and sophisticated model for producing and distributing propaganda as the Islamic State (IS), relying on digital participation from supporters on a global scale. In 2015, IS and its supporters started using the encrypted application Telegram. On pro-IS channels, supporters are currently managing virtual communities in which an ideological bolstering and recontextualization of official propaganda are apparent on a daily basis. Through a digital ethnographic approach and covert observation of IS’s official and supporter channels on Telegram for six months in 2017, this article aims to present findings on what characterizes the symbiotic relationship between official IS channels and supporter (pro-IS) channels and content. The conjunctures and collaborative media practices and affordances surrounding official and supporter channels on Telegram are discussed as manifestations of contemporary digital warfare. In addition, this article provides a wider theoretical understanding of IS’s use of Telegram as an expression of a participatory media culture in which the contemporary relationship between the IS’s central organization and its supporters constitutes a significant shift in modern online terrorism.