The plasma membrane and the underlying cortical actin cytoskeleton work together to dynamically organize and shape cells. A family of proteins, known as ezrin-radixin-moesin (ERM) physically link the membrane to the actin cortex to generate structures like microvilli at the apical surface of epithelial cells. ERM activation is dependent on PI(4,5)P2 and requires phosphorylation at a conserved C-terminal threonine residue. While many kinases have been implicated in phosphorylating ERM proteins, in this work, we show that the homologs LOK and SLK are the major mammalian ERM kinases. Knocking out all ERM proteins or LOK/SLK in human cells using CRISPR/Cas9 show strikingly similar phenotypes in interphase cells, including loss of microvilli, re-distribution of junctional actin, and ectopic myosin-II containing apical contractile structures. Further, ERM proteins negatively regulating RhoA-GTP at the apical domain, which represents a novel local feedback loop necessary for the proper apical morphology of epithelial cells. Upon live-cell imaging of ERM knockout cells, loss of ezrin results in defects in mitotic progression and astral microtubule attachment to the cell cortex. Surprisingly ThrT567 is not sufficient to rescue these defects. This led to the identification of a novel Ser539 phosphosite, which paired with T567 phosphorylation can rescue the mitotic defects. Moreover, my data suggests that ERM-dependent astral microtubule attachments act as an additional layer of activation to the mitotic checkpoint response. Collectively, this body of work offers insights into how ERM proteins regulate apical actin organization and consequently affect cell morphology and accurate cell division.