After McKay's death in 1970, Dyer was returned to a position as an Assistant to the Twelve Apostles, and later to the First Quorum of the Seventy when it was reconstituted in 1976.

Dyer is the only person in the LDS Church's history to serve in the First Quorum of Seventy after having been ordained to the office of Apostle.

Eventually, he formed the Dyer Distributing Company which he owned until 1954, when he dissolved all his business interests upon being called to full-time service as a mission president for the church.

In addition to his service as a general authority, Dyer served in many capacities within the church, including bishop and stake high councilor.

In 1961, Dyer taught that the reason most negroes were prohibited from being ordained to priesthood offices was because they were descended from Cain and thus were a "cursed lineage".