In October 1880, LDS Church president John Taylor called Smith to be a member of the Quorum of the Twelve Apostles. On October 27 of that year, he was ordained an apostle by Wilford Woodruff, who at that time was the quorum president. Smith served in that capacity until the death of First Presidency member John R. Winder in 1910; he was then asked by church president Joseph F. Smith to take Winder's place as a member of the First Presidency. John Henry Smith served in this capacity until his death the next year.