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Interspecific hybridization is a common and effective strategy for producing disease resilient citrus cultivars, including those with tolerance to Huanglongbing (HLB) disease. Several HLB-tolerant cultivars have been developed through hybridization of mandarins (Citrus reticulata) with their wild relativePoncirus trifoliata. One such cultivar, ‘US-897’, exhibits robust tolerance to the bacteria causing HLB disease,Candidatus Liberibacter asiaticus(CLas). To explore the genetic architecture of the early transcriptional response toCandidatusLiberibacter asiaticus (CLas) infection in ‘US-897’, we performed transcriptomic analysis of the hybrid and its parents, ‘Cleopatra’ (C. reticulata) and ‘Flying Dragon’ (P. trifoliata). A haplotype-resolved genome for ‘US-897’ was generated using PacBio HiFi sequencing reads to support quantification of the expression of both theCitrus and Poncirusalleles. By profiling gene expression in this parent-offspring trio, we were able to determine the mode of inheritance for genes differentially expressed between parents (‘Cleopatra’ and ‘Flying Dragon’) and their interspecific hybrid (‘US-897’), with the majority genes exhibiting non-additive patterns of gene expression inheritance. Additionally, analysis of allele-specific expression in the hybrid ‘US-897’ revealed the contribution of cis- versus trans-acting regulatory variants on genes with additive and non-additive modes of inheritance. A strong correlation between differential expression between parents and allele-specific expression in ‘US-897’ suggests that cis-regulatory variation is a significant source of expression divergence between species. Finally, genes responsive to infection withCLas were identified to explore how gene regulation associated with tolerance to HLB was rewired betweenCitrusand its relativePoncirus.