Integral to the reproductive processes of the biota of several forest, shrub, and grassland biome-types, wildfire ignites some 3,400,000km2 of Earth’s vegetated surface annually. Though a highly complex phenomena coupled with not one, but several Earth systems, human actions are both directly and indirectly changing wildfire frequencies, intensities, severities, and behaviours, and to the detriment of both environment and society. Nowhere is this felt more so than the wildland urban interface, which home to roughly 1/3 of the nation’s populous and 40% of its housing stock, is the fastest-growing land-use type in the conterminous United States. A place where fire-averse architectures meet increasingly fire-prone lands, loss of lives, properties, and livelihoods to a series of wildfire complexes of proportions unprecedented in living memory have rendered there an urgent need to reconsider the challenge of living with wildfire as a vital landscape process. The product of a transdisciplinary study which converged state-of-the-knowledge from fields as diverse as the fire, ecological, and wider Earth sciences; information, communication, computing, and related technologies, both digital and biological; evolutionary, smart and living materials, architectures, and urban systems; philosophy, anthropology, psychology, and policymaking, this thesis presents a new wildland urban interface paradigm modelled on the biochemistries, behaviours, and systems of fire-adapted flora and the fire regimes they form. Migrating biomimetics from the level of species to systems, relying not on generic notions of nature and its workings, nor assumptions more generally, but on rigorous interrogation of the interplay between biotic and abiotic processes from the molecular to landscape to planetary scale, and across both human and geological timescales, several original theoretical and technical architectural and urban concepts are discussed, together with their possible applications and implications both within and beyond the wildland urban interface. Integrating insights from local and global indigenous and ancient fire cultures, the findings conclude that not merely is a reconciliation of human and non-human systems at the interface of fire-prone wild and urban lands possible, but therein resides potent ecological, social, and technical potentialities that merit further research in the years ahead.