Hunter was born in Boise, Idaho. His father was not a Latter-day Saint (he joined the church in 1927) and would not let him get baptized until he was 12; Hunter was not ordained to the Aaronic priesthood until he was 15. He was the second person to become an Eagle Scout in the state of Idaho.

In March 1923 the Boise Ward where Hunter had been a member since baptism was split, and he ended up in the new Boise 2nd Ward. It initially met in a Jewish Synagogue that was provided free of charge. When a short time later calls were issued to build the Boise LDS Tabernacle, Hunter was the first to pledge money for the building, offering $25.

Hunter had a love for music and played the piano, violin, drums, saxophone, clarinet, and trumpet. He formed a band called Hunter's Croonaders, which played on cruise ships.

In 1928 Hunter tried an advertising system where he would publish train and bus schedules and charge for advertising, then placing them in hotels. The project worked moderately well in such cities as Nampa and Twin Falls but completely failed in Pocatello, Idaho. After this failure Hunter moved to southern California.

In California Hunter initially worked in a citrus factory and in shoe sales. After a few weeks he secured a job at a Bank of Italy branch on April 23, 1928. Hunter studied at the American Institute of Banking while working for the Bank of Italy.

In June of 1928 Hunter met Clara May "Claire" Jeffs, a lady from Salt Lake City who had moved with her family to Los Angeles in 1926. They dated some over the next year, but not exclusively with each other at this point Besides working in banking Hunter was still playing the saxophone for dances on a regular basis. By the summer of 1929 Howard and Claire were dating steady. However Howard was contemplating serving a mission so they held off on marriage. However, he eventually decided to get married instead. Howard and Claire were married in the Salt Lake Temple on June 10, 1931.

In November 1930 Howard was involved in booking for the merger of the Bank of Italy with the Bank of American of California to form the Bank of American National Trust and Savings Association. Shortly after that Hunter took a position as a junior officer with the First Exchange Bank of Inglewood. This bank was taken over by the state of California and placed in receivership in January 1932.

For the next two years Hunter filled several odd jobs, including working as a bridge painter and a laundry detergent peddler. In 1934 he managed to get a position as a title examiner with the Los Angeles County Flood Control District.

Hunter then began to study at Southwestern Law School. Howard and Claire's first son, William, died shortly after he started law school. However his sons Richard Hunter and John Hunter were both born while he was in law school.

Prior to his call as an apostle Hunter held several leadership positions in the LDS Church. He was the first president of the Pasadena, California stake of the Church, where he had also served as a bishop.

Some of his major contributions include the creation of the church's 2000th stake and his negotiations to acquire land in Jerusalem to build the BYU Jerusalem Center, which he later dedicated. Other significant activities he was involved in include the drafting of the Proclamation on the Family. In 1985, Hunter was named Acting President of the Quorum of the Twelve, in recognition of the infirmity of Marion G. Romney, who had succeeded as President of the Twelve by seniority; Hunter became president of the Quorum of the Twelve on Romney's death in 1988.

Hunter encouraged and emphasized Christlike living and temple attendance, and dedicated two temples during his administration, the Orlando Florida Temple and later the Bountiful Utah Temple shortly before he died.

Hunter served in several LDS Church assignments not directly related to ecclesiastical matters while a member of the Quorum of the Twelve. He was a member of the Board of Trustees of Brigham Young University and closely involved with the founding of the J. Reuben Clark Law School. He also was a member of the Board of Trustees of the New World Archaeology Foundation, chairman of the board of the Polynesian Cultural Center and president of the Genealogical Society of Utah.

After the death of Hunter's first wife, Clara May Jeffs in 1983, he married Inis Stanton in 1990 while president of the Quorum of the Twelve Apostles.

Both of Hunter's sons who lived to adulthood became lawyers.

When Hunter was four years old, he was stricken with polio, which afflicted his back so that he was never able to bend forward and touch the ground again.

While president of the Quorum of the Twelve, he had major health problems for the remainder of his life, including a heart attack, broken ribs from a fall at general conference, heart bypass surgery, bleeding ulcers, and a kidney failure that revived. Hunter was admitted to LDS Hospital on January 9, 1995 for exhaustion and was released on January 16. While hospitalized, it was discovered that Hunter was suffering from prostate cancer that had spread to the bones.

Hunter died in his downtown Salt Lake City, Utah residence after a battle with prostate cancer. He was 87. With the church leader at the time of his death were his wife, Inis; his nurse, who had been attending him; and his personal secretary, Lowell Hardy. Funeral services were held on March 8, 1995 at the Salt Lake Tabernacle under the direction of Gordon B. Hinckley. Hunter was buried in the Salt Lake City Cemetery. On October 14, 2007 at her home in Laguna Hills, California, his wife Inis Stanton Hunter died of causes incident to age.

[[Image:HowardWHunterGrave.jpg|right|thumb|200px|Grave marker of Howard W. Hunter.]]

While preparing to speak at a CES fireside being held at Brigham Young University's Marriott Center on February 7, 1993, Hunter was confronted by Cody Judy, who rushed onto the rostrum and threatened Hunter and the audience of 15,000—17,000. Judy carried a briefcase that he claimed contained a bomb and held what appeared to be a detonator-like device. Judy demanded that Hunter read a three-page document that supposedly detailed God's plan for Judy to lead the church, which Hunter refused to do. The audience spontaneously sang "We Thank Thee, O God, for a Prophet", during which students from the audience and then security personnel overtook Judy. After Judy was taken away, Hunter delivered his prepared remarks, a talk entitled "An Anchor to the Souls of Men."