Huanglongbing (HLB) and citrus canker are two major destructive bacterial diseases in the citrus industry caused by Candidatus Liberibacter asiaticus (CLas) and Xanthomonas citri subsp. citri (Xcc), respectively. ABI5 transcription factors are crucial for plant growth and development as well as for responses to various abiotic and biotic stresses, including viruses and fungi. This study aimed to identify and characterize ABI5 genes in the Citrus sinensis genome and investigate their functions in response to CLas and Xcc infections. We identified five putative CsABI5 genes on three citrus chromosomes, designated CsABI5-1 through CsABI5-5, which share high identity with Arabidopsis ABI5 subfamily proteins and function in the nucleus. The expression of CsABI5s was differentially altered in citrus leaves under HLB and citrus canker stress, as well as in response to exogenous phytohormones. Notably, CsABI5-5 was upregulated by abscisic acid (ABA), salicylic acid (SA), and ethylene, whereas it was downregulated by methyl jasmonate, CLas, and Xcc. Overexpression of CsABI5-5 inhibited the propagation of CLas in citrus hairy roots and reduced leaf susceptibility to Xcc. This resistance was associated with increased levels of SA, jasmonic acid, callose, and reactive oxygen species, along with decreased ABA, compared to non-transgenic samples. This study highlights the critical role of CsABI5-5 in regulating plant resistance to biotic stresses and demonstrates its potential utility as a powerful gene for biotechnology-assisted plant breeding aimed at improving citrus resistance to bacterial diseases.