Although the phylumChloroflexotais ubiquitous, its biology and evolution are poorly understood due to limited cultivability. Here, we isolated two motile, thermophilic bacteria from hot spring sediments belonging to the genusTepidiformaand classDehalococcoidiawithin the phylumChloroflexota. A combination of cryo-electron tomography, exometabolomics, and cultivation experiments using stable isotopes of carbon revealed three unusual traits: flagellar motility, a peptidoglycan-containing cell envelope, and heterotrophic activity on aromatics and plant-associated compounds. Outside of this genus, flagellar motility has not been observed inChloroflexota, and peptidoglycan-containing cell envelopes have not been described inDehalococcoidia. Although these traits are unusual among cultivatedChloroflexotaandDehalococcoidia, ancestral character state reconstructions showed flagellar motility and peptidoglycan-containing cell envelopes were ancestral within theDehalococcoidia, and subsequently lost prior to a major adaptive radiation ofDehalococcoidiainto marine environments. However, despite the predominantly vertical evolutionary histories of flagellar motility and peptidoglycan biosynthesis, the evolution of enzymes for degradation of aromatics and plant-associated compounds was predominantly horizontal and complex. Together, the presence of these unusual traits inDehalococcoidiaand their evolutionary histories raise new questions about the timing and selective forces driving their successful niche expansion into global oceans.