Zetaproteobacteria have been reported in different marine and terrestrial environments all over the globe. They play an essential role in marine iron-rich microbial mats, as one of their autotrophic primary producers, oxidizing Fe(II) and producing Fe-oxyhydroxides with different morphologies. Here, we study and compare the Zetaproteobacterial communities of iron-rich microbial mats from six different sites of the Lucky Strike Hydrothermal Field through the use of the Zetaproteobacterial operational taxonomic unit (ZetaOTU) classification. We report for the first time the Zetaproteobacterial core microbiome of these iron-rich microbial mats, which is composed of four ZetaOTUs that are cosmopolitan and essential for the development of the mats. The study of the presence and abundance of different ZetaOTUs among sites reveals two clusters, which are related to the lithology and permeability of the substratum on which they develop. The Zetaproteobacterial communities of cluster 1 are characteristic of poorly permeable substrata, with little evidence of diffuse venting, while those of cluster 2 develop on hydrothermal slabs or deposits that allow the percolation and outflow of diffuse hydrothermal fluids. In addition, two NewZetaOTUs 1 and 2 were identified, which could be characteristic of anthropic iron and unsedimented basalt, respectively. We also report significant correlations between the abundance of certain ZetaOTUs and that of iron oxide morphologies, indicating that their formation could be taxonomically and/or environmentally driven. We identified a new morphology of Fe(III)-oxyhydroxides that we named “corals.” Overall, our work contributes to the knowledge of the biogeography of this bacterial class by providing additional data from the Atlantic Ocean, a lesser-studied ocean in terms of Zetaproteobacterial diversity. IMPORTANCE Up until now, Zetaproteobacterial diversity studies have revealed possible links between Zetaproteobacteria taxa, habitats, and niches. Here, we report for the first time the Zetaproteobacterial core microbiome of iron-rich mats from the Lucky Strike Hydrothermal Field (LSHF), as well as two new Zetaproteobacterial operational taxonomic units (NewZetaOTUs) that could be substratum specific. We highlight that the substratum on which iron-rich microbial mats develop, especially because of its permeability to diffuse hydrothermal venting, has an influence on their Zetaproteobacterial communities. Moreover, our work adds to the knowledge of the biogeography of this bacterial class by providing additional data from the hydrothermal vent sites along the Mid-Atlantic Ridge. In addition to the already described iron oxide morphologies, we identify in our iron-rich mats a new morphology that we named corals. Finally, we argue for significant correlations between the relative abundance of certain ZetaOTUs and that of iron oxide morphologies, contributing to the understanding of the drivers of iron oxide production in iron-oxidizing bacteria.