Root-knot nematode (RKN) causes severe yield loss in cucumber. Understanding the interactions of biocontrol agent–soil microbiomes and RKNs is essential for enhancing the efficacy of biocontrol agents and nematicides to curb RKN damage to cucumber. The field experiment in this work was conducted to determine the ability of Bacillus velezensis GHt-q6 to colonize cucumber plants, investigate its effect on the control of RKNs, and assess its influence on soil microbiology in the inter-root zone of cucumber plants. After 10 days post-treatment (DPT), GHt-q6-Rif could stably colonize the roots (4.55 × 10⁴ cfu·g⁻¹), stems (3.60 × 10³ cfu·g⁻¹), and leaves (3.60 × 10² cfu·g⁻¹) of cucumber. The high-throughput sequencing results suggested that the bacterial community diversity increased at the late development phase (p > 0.05). The strain GHt-q6 increased the relative abundance of beneficial bacteria (Gemmatimonadaceae, Sphingomonadaceae, Pseudomonadaceae). Throughout the complete cucumber growth period, strain GHt-q6 significantly increased soil urease, sucrase, accessible potassium, and phosphorus (p < 0.05). However, strain GHt-q6 had a minimal effect on catalase activity. At the pulling stage, strain GHt-q6 exhibited 43.35% control effect on cucumber RKNs, which was 7.54% higher than that of Bacillus subtilis. The results highlighted the significant potential of the strain GHt-q6 to manage cucumber RKNs and improve soil microecology. Hence, the applications of B. velezensis GHt-q6 can enhance the nematicidal action to curb RKN infecting cucumber.