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 during the Thirty-fourth Congress, serving from February 4, 1856, until December 6, 1857. During discussions on secession, Cullom campaigned in Tennessee to keep his state in the Union but when Tennessee officially seceded, he reluctantly supported the decision and returned home at Carthage, taking a less prominent stance thereafter.