Phytopathogenic oomycetes, particularly Phytophthora capsici, the causal agent of Phytophthora blight disease in essential vegetables and fruit crops, remains a persistent challenge in the vegetable production industry. However, the core molecular regulators of the pathophysiology and broad-range host characteristics of P. capsici remain unknown. Here, we used transcriptomics and CRISPR-Cas9 technology to functionally characterize the contributions of a novel gene (PcTBCC1) coding for a hypothetical protein with a tubulin-binding cofactor C domain with a putative chloroplast-targeting peptide (cTP) to the pathophysiological development of P. capsici. We observed significant upregulation in the expression of PcTBCC1 during pathogen–host interactions. However, the vegetative growth of the ∆Pctbcc1 strains was not significantly different from the wild-type strains. PcTBCC1 gene replacement significantly compromised the sporulation, pathogenic differentiation, and virulence of P. capsici. At the same time, ∆Pctbcc1 strains were sensitive to cell wall stress-inducing osmolytes. These observations, coupled with the close evolutionary ties between PcTBCC1 and pathogenic oomycetes and algae, partly support the notion that PcTBCC1 is a conserved determinant of pathogenesis. This study provides insights into the significance of tubulin-binding cofactors in P. capsici and underscores the potential of PcTbcc1 as a durable target for developing anti-oomycides to control phytopathogenic oomycetes.