Phytophthora gummosis, foot rot, and root rot are considered major challenges to the citrus industry worldwide. Little is known about the Phytophthora–microbiome interaction, despite several studies demonstrating changes in the microbial composition of the rhizosphere following challenges by a pathogen. In the present study, we studied the microbial diversity and community structure in healthy rhizospheres and Phytophthora-infected rhizospheres of Khasi mandarin (Citrus reticulata Blanco), a commercial cultivar extensively grown in the northeast of India. An exploratory study was conducted to identify Phytophthora-infected orchards of Khasi mandarin, and the isolated pathogen was confirmed as P. nicotianae based on its morpho-cultural and molecular characteristics coupled with pathogenicity tests. This study on culturable microbes established the dominance of Trichoderma spp. in the healthy rhizosphere, while the diseased rhizosphere showed the presence of Fusarium spp. A metagenomic study further revealed that the rhizospheres of Phytophthora-infected plants were dominated by species such as Bacteroidia spp., Patescibacteria spp., and Pythium spp., while the healthy Khasi mandarin rhizospheres had a more diverse community predominantly represented by Trichoderma, Penicillium, Linnemannia, Mortierella, Talaromyces, Saitozyma, Bacteroidetes, Pseudomonas, Cytophagia, Cyanobacteria, Bacteroidia, Sphingobacteriia, Burkholderia, Bacillus, and Bradyrhizobium. Terrabacteria and FCB (Fibrobacterota, Chlorobiota, and Bacteroidota groups) were found to exist in higher relative abundance in disease-free soils than in Phytophthora-infected soils, while phylum Proteobacteria showed identical relative abundance in all soil types. The phyla represented by Pseudomonas, Flavobacteriia, Candidatus, Mycobacterium, Rhizobium, Mesorhizobium, Sphingomonas, and Cytophagia were the most common bacterial phyla in all soil samples, but healthy soil exhibited a greater abundance of Bacteroidetes, Pseudomonas, Cytophagia, Cyanobacteria, Bacteroidia, Sphingobacteriia, Burkholderia, Bacillus, and Bradyrhizobium. Our study suggests that the presence of Phytophthora spp. in the rhizosphere alters microbial community structure, having potentially strong implications for plant health and productivity. These rhizosphere microbiome-derived citrus responses shed light on exploring effective management strategies for Phytophthora gummosis disease ailing Khasi mandarin.