Background: The chicken is the most abundant food animal in the world. However, despite its importance, the chicken gut microbiome remains largely undefined. Here, we exploit culture-independent and culture-dependent approaches to deliver a genomic blueprint of this complex microbial community. Results: We performed metagenomic sequencing of fifty chicken faecal samples from two breeds and analysed these, alongside all (n=582) relevant publicly available chicken metagenomes, to cluster over 20 million non-redundant genes and to construct over 5,500 metagenome-assembled bacterial genomes. In addition, we recovered nearly 600 bacteriophage genomes This represents the most comprehensive view of the chicken gut associated microbiome to date, encompassing dozens of novel candidate bacterial genera and hundreds of novel candidate species. Keen to provide a stable, clear and memorable nomenclature for novel species, we devised a scalable combinatorial system for the creation of hundreds of well-formed Latin binomials. We cultured bacterial isolates from faeces to deliver 282 whole genome sequences, incorporating thirty novel species, together with three species from the genus Escherichia, including the newly named species Escherichia whittamii.Conclusions: Our metagenomic and culture-based analyses provide new insights into the bacterial, archaeal and bacteriophage components of the chicken gut microbiome. The resulting datasets expand the known diversity of the chicken gut microbiome and provides a key resource for future high-resolution taxonomic and functional studies on the chicken gut microbiome.