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Plant cell wall (CW) integrity signaling enables early detection of microbial invasion, yet the receptors involved and their spatial and temporal dynamics during infection remain largely unknown. We identify ATHENA (ATHE)/MEE39, a previously uncharacterized malectin-like leucin-rich repeat receptor kinase (Mal-LRR-RK) that contributes to defense against the root vascular pathogen Fusarium oxysporum (Fo), particularly in outer root layers where colonization begins. ATHE abundance, localization, and endocytic trafficking are rapidly remodeled during infection, and loss of ATHE compromises basal immunity and early pathogen-induced transcriptional reprogramming. ATHE responds to altered cellulose synthesis, cellulose-derived oligosaccharides, mechanically induced CW perturbations, and the fungal secreted peptide Fo-RALF. In most of these contexts, ATHE acts together with the LRR-RK MIK2, forming a pathogen-strengthened RK complex that fine-tunes root responses to Fo. This represents the first example of a receptor complex visualized subcellularly in vivo during a plant-microbe interaction. Although Brassicaceae -specific, heterologous expression of ATHE enhanced tomato resistance to Fo, highlighting its functional relevance across plant lineages and its potential use for crop engineering. Our work reveals a previously unrecognized strategy by which plants decode microbial threats through dynamic CW-integrity surveillance.