Problematic drug use is a growing problem in South African urban spaces. In Durban, as in other cities in the country, the dominant response of the capital-oriented Municipality has been to make drug use invisible through prohibition and a promotion of abstinence approaches. This governance mentality and technology has failed dismally, evidenced in the rise of street-level heroin use. During the COVID-19 hard lockdown, the municipality was forced to re-examine its governance approach to drug use, taking guidance from non-state actors in an attempt to more effectively reduce the harms associated with drug use. In tracing the historical contestations around street-level drug use in Durban, this paper shares the untold story of how, when prompted by an unforeseen crisis, a municipality was able to successfully shift its mentality and technology in governing street-level drug use. Drawing conceptually on nodal governance theory and the quadruple helix approach, it reveals the complexities of urban governance processes and demonstrates the power of political opportunities, the transformative role of unexpected consequences, and the importance of informed political leadership. It also shows how multi-stakeholder partnership projects can be a useful mechanism not only to implement innovative and creative policy goals, but also to build robust relationships to navigate the manifestation of informal urbanism. It also calls for governing through harm minimisation rather than through actuarial risk management approaches that are closely associated with a neoliberal agenda.