Ediacara fossils [575 to 542 million years ago (Ma)] represent Earth’s oldest known complex macroscopic life forms, but their morphological history is poorly understood. A comprehensive quantitative analysis of these fossils indicates that the oldest Ediacara assemblage—the Avalon assemblage (575 to 565 Ma)—already encompassed the full range of Ediacara morphospace. A comparable morphospace range was occupied by the subsequent White Sea (560 to 550 Ma) and Nama (550 to 542 Ma) assemblages, although it was populated differently. In contrast, taxonomic richness increased in the White Sea assemblage and declined in the Nama assemblage. These diversity changes, occurring while morphospace range remained relatively constant, led to inverse shifts in morphological variance. The Avalon morphospace expansion mirrors the Cambrian explosion, and both events may reflect similar underlying mechanisms.