Environmental fluctuations in redox may reinforce rather than hinder evolutionary transitions, such that variability in near‐surface oceanic oxygenation can promote morphological evolution and novelty. Modern, low‐oxygen regions are heterogeneous and dynamic habitats that support low diversity and are inhabited by opportunistic and non‐skeletal metazoans. We note that several major radiation episodes follow protracted or repeating intervals (>1 million years) of persistent and dynamic shallow marine redox (oceanic anoxic events). These are also often associated with short‐lived mass‐extinction events (<0.5 million years) where skeletal benthic incumbents are removed, and surviving or newly evolved benthos initially inhabit transient oxic habitats. We argue that such intervals create critical opportunities for the generation of evolutionary novelty, followed by innovation and diversification. We develop a general model for redox controls on the distribution and structure of the shallow marine benthos in a dominantly anoxic world, and compile data from the terminal Ediacaran–mid‐Cambrian (∼560–509 Ma), late Cambrian–Ordovician (∼500–445 Ma), and Permo‐Triassic (∼255–205 Ma) to test these predictions. Assembly of phylogenetic data shows that prolonged and widespread anoxic intervals indeed promoted morphological novelty in soft‐bodied benthos, providing the ancestral stock for subsequently skeletonized lineages to appear as innovations once oxic conditions became widespread and stable, in turn promoting major evolutionary diversification. As a result, we propose that so‐called ‘recovery’ intervals after mass extinctions might be better considered as ‘innovation’ intervals.