Cullom was appointed the Clerk of the United States House of Representatives in the Thirty-fourth Congress, and he served from February 4, 1856, to December 6, 1857. During the debate on secession, Cullom stumped Tennessee in favor of remaining in the Union but when Tennessee finally seceded, he grudgingly supported the decision but retired to his home at Carthage and did not take a prominent role supporting either side.
Cullom was appointed Clerk of the United States House of Representatives in the Thirty-fourth Congress, serving from February 4, 1856, to December 6, 1857. During debates on secession, Cullom campaigned in Tennessee for Union membership but when Tennessee ultimately seceded, he reluctantly supported the decision and retired to Carthage, playing a minor role thereafter.