McConkie was a member of the First Council of the Seventy of the LDS Church from 1946 until his calling to the Quorum of the Twelve Apostles.

During his time as a general authority, McConkie published several doctrinal books and articles and wrote the chapter headings of the LDS Church's 1979–81 editions of the standard works.

In 1936, McConkie participated in the first Hill Cumorah Pageant, which was attended by his future father-in-law, Joseph Fielding Smith.

McConkie graduated with a bachelor of laws degree in 1939 and was third out of seventy-five on the Utah bar exam.

While covering the proceedings of LDS general conference on October 6, 1946, McConkie was interviewed by apostle David O. McKay to fill a vacancy in the First Council of the Seventy created by the death of John H. Taylor.

McConkie's name was presented for a sustaining vote by the membership of the church that same day, and on October 10, he was ordained and set apart by George Albert Smith.

In 1958, McConkie published a book, Mormon Doctrine: A Compendium of the Gospel, which he described as "the first major attempt to digest, explain, and analyze all of the important doctrines of the kingdom" and "the first extensive compendium of the whole gospel—the first attempt to publish an encyclopedic commentary covering the whole field of revealed religion."

[5] In writing the book, McConkie relied heavily upon the church's standard works and recognized doctrinal authorities.

Apostle Mark E. Petersen called it "full of errors and misstatements, and it is most unfortunate that it has received such wide circulation.

[5] Mormon Doctrine remained in print until 2010, when Deseret Book ceased publication, citing poor sales.

Their daughter, Vivian, was married and son, Joseph, was serving a mission in Scotland, so six of their children accompanied them to Australia.

In October 1962, McConkie reported "an all-time high mark in mission converts and willingness of members to build new chapels....

When asked why they contributed to the company, close to half mentioned trust in McConkie or other LDS Church leaders specifically.

[10] Joseph Fielding Smith, McConkie's father-in-law, who had been serving as church president, died on July 2, 1972.

[13] McConkie also wrote the fourth verse to "Come, Listen to a Prophet's Voice" which is hymn #21 in the church's 1985 hymnal.

"[19] McConkie states that the Jews' rejection of Jesus is the cause of historical persecution of the Jews: "Let the spiritually illiterate suppose what they may, it was the Jewish denial and rejection of the Holy One of Israel, whom their fathers worshiped in the beauty of holiness, that has made them a hiss and a byword in all nations and that has taken millions of their fair sons and daughters to untimely graves.

"[19] One of the most controversial topics that McConkie defended in his writings was the church's policy of denying the priesthood to men of African descent until 1978.

In 1958, McConkie wrote: In the pre-existent eternity various degrees of valiance and devotion to the truth were exhibited by different groups of our Father's spirit offspring.

[5]McConkie extended the analysis to conclude that God had established a caste system that proscribed intermarriage of other races with the "negro race," which McConkie believed to be descended from Cain, the murderer of Abel: "In a broad general sense, caste systems have their root and origin in the gospel itself, and when they operate according to the divine decree, the resultant restrictions and segregation are right and proper and have the approval of the Lord.

To illustrate: Cain, Ham, and the whole negro race have been cursed with a black skin, the mark of Cain, so they can be identified as a caste apart, a people with whom the other descendants of Adam should not intermarry.”[20] On June 1, 1978, McConkie was present in the Salt Lake Temple when a revelation was received by the First Presidency and the Twelve "that the time had now come to extend the gospel and all its blessings and all its obligations, including the priesthood and the blessings of the house of the Lord, to those of every nation, culture and race, including the black race.

McConkie's earlier statements on the topic, like those of other church leaders, implied or stated that the priesthood restriction would never be lifted.

Forget everything that I have said, or what President Brigham Young or George Q. Cannon or whoever has said in days past that is contrary to the present revelation.