The coronavirus disease 2019 (Covid-19) condition has prompted serious questions about the challenges faced by the established two-century-old canons of education in architecture and urbanism. This paper establishes an evolutionary account on how design education in architecture and urbanism has arrived at the pre-Covid-19 condition, explores current challenges and, in the process of encountering the Covid-19 condition, asks the question of what the scope of opportunities is to meet these challenges. A chronological analysis of design pedagogy is undertaken to instigate a debate on its future in a post-pandemic environment. This paper captures the salient characteristics of the legacy model that is inherited from historical schools, demonstrates the influence of and resistance to this model (1960s); identifies the qualities of various alternatives including ten ground-breaking alternative pedagogies (1970s–1990s); highlights strengths of further alternative approaches including critical inquiry, the process-based and learning-by-making pedagogies (2000s) and the social construction-based pedagogies (2010s). Scrutinising the consequences of the Covid-19 condition and the associated ‘transitional emergency model’, the analysis articulates the persisting challenges and examines current adaptations while outlining the scope of future opportunities for a responsive design pedagogy in architecture and urbanism for a post-pandemic world.