Inflammatory bowel disease (IBD), including Crohn's disease and ulcerative colitis, is considered significant global health concerns worldwide. Many studies have demonstrated that environmental and dietary factors influence the gut microbiota, which in turn orchestrates the host immune responses. These interactions are also involved in complex metabolic processes that contribute to the pathogenesis of IBD. Furthermore, recent studies in genomics and metabolomics have unveiled the intricate relationship between microbial influencers and host epigenetics. The dynamics of gut microbiota and its metabolites intricately align with DNA methylation, histone methylation, lactylation, glycosylation, and non-coding RNAs, which are key players in epigenetics. Here, we summarize and discuss the complex interplay among gut microbiota, epigenetics, and environmental and dietary factors, and their impact on the pathogenesis of IBD. Furthermore, we highlight the importance of multi-omics technologies in dissecting the host-microbe interactions in IBD, potentially offering a framework for developing effective treatment strategies.