Oaks was born in Provo, Utah to Stella Harris and Dr. Lloyd E. Oaks. His father died when Dallin was eight years old.

He graduated from Brigham Young High School in 1950, Brigham Young University in accounting in 1954, and the University of Chicago Law School in 1957.

After receiving his Juris Doctor from the University of Chicago Law School, Oaks clerked for Chief Justice Earl Warren of the United States Supreme Court from 1957 to 1958. After his clerkship he practiced at the law firm of Kirkland & Ellis in Chicago. Oaks left Kirkland & Ellis to become a professor at the University of Chicago Law School. During part of his time on the faculty of the Law School, Oaks served as interim dean. Oaks left the Law School upon being appointed President at Brigham Young University.

Oaks would also serve five years as chairman of the Board of Directors of the Public Broadcasting Service (PBS) (1979—1984) and eight years as chairman of the Board of Directors of the Polynesian Cultural Center.

President of Brigham Young University

Oaks served as president of Brigham Young University from 1971—1980. As president of Brigham Young University, Oaks oversaw the start of the J. Reuben Clark Law School and the Graduate Business School. Although university enrollment continued to grow and new buildings were added, neither were done at the pace of the previous administration under Ernest L. Wilkinson.

Upon leaving Brigham Young University, Oaks was appointed as a justice in the Utah Supreme Court. He would serve in this capacity from 1980 to 1984, when he resigned to accept a call by the LDS Church to become a member of the Quorum of the Twelve Apostles.

Considered as Supreme Court nominee

In 1976, Oaks was listed by U.S. attorney general Edward H. Levi among potential Gerald Ford Supreme Court candidates. In 1981, he was closely considered by the Ronald Reagan administration as a Supreme Court nominee.

LDS Church apostle

On May 3, 1984, Oaks was sustained an apostle and a member of the Quorum of the Twelve Apostles in the LDS Church. He was the youngest apostle by years at that time, and the youngest man to be called since Boyd K. Packer, who was called in 1970 at age 45. As a member of the Quorum of the Twelve, Oaks is accepted by the church as a prophet, seer, and revelator.

Oaks was ordained as a member of the Quorum of the Twelve on April 7, 1984, with fellow quorum member Russell M. Nelson. His ordination was delayed a month to allow him to resign from his judgeship before assuming his place in the Quorum.

Between 2002 and 2004, Oaks presided over the church area in the Philippines. This assignment was unusual because responsibility for presiding over areas of the LDS Church is generally delegated to members of the Quorums of the Seventy.

Family

Oaks was married to June Dixon Oaks on June 24, 1952. She died on July 21, 1998. They had six children. Among these is Dallin D. Oaks, a linguistics professor at Brigham Young University, and Jenny Oaks Baker, a musician and artist. On August 25, 2000, Dallin H. Oaks married Kristen Meredith McMain in the Salt Lake Temple.

As a law professor, Oaks focused his scholarly research on the writ of habeas corpus and the exclusionary rule. In California v. Minjares, Justice William Rehnquist, in a dissenting opinion, wrote "[t]he most comprehensive study on the exclusionary rule is probably that done by Dallin Oaks for the American Bar Foundation in 1970. According to this article, it is an open question whether the exclusionary rule deters the police from violating Fourth Amendment protections of individuals.

Oaks also undertook a legal analysis of the Nauvoo City Council's actions against the Nauvoo Expositor. He opined that while the destruction of the Expositor's printing press was legally questionable, under the law of the time the newspaper certainly could have been declared libelous and therefore a public nuisance by the Nauvoo City Council. As a result, Oaks concludes that while under contemporaneous law it would have been legally permissible for city officials to destroy, or "abate," the actual printed newspapers, the destruction of the printing press itself was probably outside of the council's legal authority, and its owners could have sued for damages.

As a Utah Supreme Court Justice from 1980 to 1984, Oaks authored opinions on a variety of topics. In In Re J. P., a proceeding was instituted on a petition of the Division of Family Services to terminate parental rights of natural mother. Oaks wrote that a parent has a fundamental right protected by the Constitution to sustain his relationship with his child but that a parent can nevertheless be deprived of parental rights upon a showing of unfitness, abandonment, and substantial neglect.

In KUTV, Inc. v. Conder, media representatives sought review by appeal and by a writ of prohibition of an order barring the media from using the words "Sugarhouse rapist" or disseminating any information on past convictions of defendant during the pendency of a criminal trial. Oaks, in the opinion delivered by the court, held that the order barring the media from using the words "Sugarhouse rapist" or disseminating any information on past convictions of defendant during the pendency of the criminal trial was invalid on the ground that it was not accompanied by the procedural formalities required for the issuance of such an order.

In Wells v. Children's Aid Soc. of Utah, an unwed minor father brought action through a guardian ad litem seeking custody of a newborn child that had been released to state adoption agency and subsequently to adoptive parents, after the father had failed to make timely filing of his acknowledgment of paternity as required by statute. Oaks, writing the opinion for the court, held that statute specifying procedure for terminating parental rights of unwed fathers was constitutional under due process clause of United States Constitution.