The museum began with an act of institutional ambition. In the early 1960s, the Country Music Association realized it needed more than a trade organization. It needed a shrine. The nonprofit Country Music Foundation was chartered by Tennessee in 1964, and CMA Executive Director Jo Walker-Meador led fundraising efforts to build a museum at the head of Music Row. Martin Jenter of Jenter Exhibits, Inc., designed the interior exhibits at his Mount Vernon, New York plant, then shipped them by moving van to Nashville. The grand opening came on April 1, 1967, in a building modeled after the National Baseball Hall of Fame in Cooperstown. A small library started in a loft above one of the galleries. It would grow into one of the most important music archives in the world.

Nashville architect Seab Tuck of Tuck-Hinton designed the downtown building with obsessive musical symbolism. The cylindrical Rotunda can be read as a drum kit, a rural water tower, or a grain silo. Its four-tiered roof represents the evolution of recording technology: the 78, the vinyl LP, the 45, and the CD. Stone bars on the Rotunda's exterior wall encode the notes of the Carter Family's classic "Will the Circle Be Unbroken," while the song's title rings the interior. Georgia yellow pine from the South's forests lines the floors. Crab Orchard stone from the East Tennessee mountains gives the Conservatory a front-porch feel. Steel beams supporting glass walls call to mind rural railroad bridges, and cascading water along the Grand Staircase evokes the rivers that connected musicians across the nation.

The museum's collections stagger the imagination. The Bob Pinson Recorded Sound Collection holds over 250,000 recordings, including an estimated 98 percent of all pre-World War II country recordings released commercially. Half a million photographs document the genre from its folk roots through today. More than 900 musical instruments fill the climate-controlled vaults, among them Mother Maybelle Carter's Gibson L-5 guitar, Bob Wills's fiddle, Chet Atkins's 1950 D'Angelico archtop, and Bill Monroe's mandolin. Elvis Presley's 1960 "Solid Gold" Cadillac limousine sits alongside Webb Pierce's 1962 Pontiac Bonneville convertible and Jerry Reed's 1980 Trans Am from Smokey and the Bandit II. The museum also operates Historic RCA Studio B on Music Row, Nashville's oldest surviving recording studio, where Elvis, Dolly Parton, and Waylon Jennings cut records.

Inside the Rotunda, bronze bas-relief plaques line the walls like notes on a staff. Each one honors a member of the Country Music Hall of Fame, the highest recognition the genre can bestow. The honor was created in 1961, and the first inductees were Hank Williams, Jimmie Rodgers, and songwriter Fred Rose. Roy Acuff became the first living inductee in 1962. No one was inducted in 1963 because no candidate received sufficient votes. The Medallion Ceremony, held annually, remains one of Nashville's most emotional events. In the Rotunda, Thomas Hart Benton's mural "The Sources of Country Music" watches over the proceedings. It was Benton's final work. He died in his studio while completing it.