Animal development is classified as conditional or autonomous based on whether cell fates are specified through inductive signals or maternal determinants, respectively. Yet how these two major developmental modes evolved remains unclear. During spiral cleavage—a stereotypic embryogenesis ancestral to 15 invertebrate groups, including molluscs and annelids—most lineages specify cell fates conditionally, while some define the primary axial fates autonomously. To identify the mechanisms driving this change, we studied Owenia fusiformis, an early-branching, conditional cleaving annelid. In Owenia, ERK1/2-mediated FGF receptor signalling specifies the endomesodermal progenitor. This cell acts as an embryonic organiser, inducing mesodermal and posterodorsal fates in neighbouring cells and repressing anteriorising signals. The organising role of ERK1/2 in Owenia is shared with molluscs, but not with autonomous cleaving annelids. Together, these findings indicate that conditional specification of an ERK1/2+ organiser is ancestral in spiral cleavage, repeatedly lost in annelid lineages as they evolved autonomous development.