Actin is an extraordinarily complex protein whose functions are essential to cell motility, division, contraction, signaling, transport, tissular structures, DNA repair, and many more cellular activities critical to life for both animals and plants. It is one of the most abundant and conserved proteins and it exists in either a soluble, globular (monomeric, G-actin) or an insoluble, self-assembled (polymerized or filamentous actin, F-actin) conformation as a key component of the cytoskeleton. In the early 1990's little, if anything, was known about the impact of reactive oxygen species (ROS) on the biology of actin except that ROS could disrupt the actin cytoskeleton. Instructively, G-actin is susceptible to alteration by ROS, and thus, purification of G-actin is typically performed in the presence of strong antioxidants (like dithiothreitol) to limit its oxidative degradation. In contrast, F-actin is a more stable conformation and thus actin can be kept relatively intact in purified preparations as filaments at low temperature for extended periods of time. Both G- and F-actin interact with a myriad of intracellular proteins and at least with a couple of extracellular proteins, and these interactions are essential to the many actin functions. This review will show how, over the past 30 years, our understanding of the role of ROS for actin biology has evolved from noxious denaturizing agents to remarkable regulators of the actin cytoskeleton in cells and consequent cellular functions.