Leveraging a suite of remote sensing technologies deployed over large areas, this paper presents results that challenge long-held ideas about the origin and development of the world’s oldest urban centers, in southern Iraq. The standard model of third millennium BCE Mesopotamian cities presents them as nuclear, compact settlements set within an irrigated agricultural hinterland, expanding continuously from a monumental religious complex. This reconstruction holds enormous influence in the comparative global study of early urbanism. UAV photos and magnetic gradiometry data captured at Lagash (Tell al-Hiba) show dense architecture and related paleoenvironmental features over c. 300 ha, revealing a city that does not conform to the standard model. Early Dynastic Lagash (2900–2350 BCE) was composed of spatially discrete sectors bounded by multiple surrounding walls and/or watercourses and separated by open spaces. The evidence is suggestive of a marshy or watery local environment, and the city sectors may have originated as marsh islands. The discontinuous, walled nature of inhabited areas would have had social and logistical ramifications for city inhabitants. A number of contemporary sites are characterized by multiple archaeological mounds, suggesting that early southern Mesopotamian cities may have frequently been spatially multi-centric.