Iron-sulfur minerals such as pyrite are found in many marine benthic habitats. At deep-sea hydrothermal vent sites they occur as massive sulfide chimneys. Hydrothermal chimneys formed by mineral precipitation from reduced vent fluids upon mixing with cold oxygenated sea water. While microorganisms inhabiting actively venting chimneys and utilizing reduced compounds dissolved in the fluids for energy generation are well studied, only little is known about the microorganisms inhabiting inactive sulfide chimneys. We performed a comprehensive meta-proteogenomic analysis combined with radiometric dating to investigate the diversity and function of microbial communities found on inactive sulfide chimneys of different ages from the Manus Basin (SW Pacific). Our study sheds light on potential lifestyles and ecological niches of yet poorly described bacterial clades dominating inactive chimney communities. Among these clades was a sulfate-reducing Nitrospirae bacterium with genomic potential for CO2 and nitrogen fixation. Most inactive chimneys, however, were dominated by metal-sulfide oxidizing autotrophic Gammaproteobacteria, which we were able to attribute to the recently described family of Woeseiaceae and the SSr clade found in marine sediments around the world. Our metaproteomic analysis identifies these gammaproteobacterial clades as autotrophic sulfide and potentially iron oxidizers in marine pyrite-rich environments such as hydrothermal vents.