Tomato late blight caused by Phytophthora infestans is a devastating disease, and current control of the disease relies heavily on chemical fungicides. Certain Trichoderma strains used as biocontrol fungi have shown superb efficacy against P. infestans and some other oomycete phytopathogens. In this study, T. paratroviride strain 8942 appeared to be effective in control of tomato late blight disease, reducing the necrosis degree of plant tissues, promoting callose deposition in tomato leaves, and increasing defense enzyme activities. RT-qPCR analysis showed that strain 8942 inhibited metabolism of salicylic acid and promoted metabolism of jasmonic acid at the early stage of colonization. In addition, root colonization of the strain significantly promoted tomato growth. Observations of rhizosphere soil properties showed that 8942 significantly increased the activities of urease, catalase, and protease, and its cell-free filtrates at low concentrations induced the accumulation of auxin in root tips. Transcriptomic data suggested the existence of a balance between biotrophic adaptation and biocontrol readiness during 8942’s interaction with tomato roots. Trichoderma paratroviride strain 8942 is promising and has potential for biological control of tomato late blight and plant growth promotion, as determined by integrated investigations of hormonal regulation, rhizosphere modulation, transcriptional reprogramming, etc.