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The first contract for construction was awarded on August 2, 1991, for the stretch between south of Stewart's Ferry Pike and south of I-40 in Lebanon, and work progressed in stages.

Contracts for two noncontiguous sections, located between I-24 and US 41/70S and SR 266 and Stewart's Ferry Pike, were awarded on July 24, 1992.

The first section of I-840, located between I-40 in Lebanon and Stewart's Ferry Pike, opened on August 2, 1995. The segment between Stewart's Ferry Pike and I-24 near Murfreesboro was completed on November 21, 1996. On November 30, 2000, the section between I-24 and US 31A/US 41A near Triune was opened. The portion between US 31A/US 41A and US 431 (Lewisburg Pike) near Franklin, including the interchange with I-65, opened on October 18, 2001. The section between I-40 near Dickson and SR 100 opened on December 5, 2002. Due to high costs and environmental concerns, the proposed northern half of I-840 was indefinitely placed on hold in 2003. The short segment between US 431 and US 31 (Columbia Pike) opened to traffic on September 9, 2005.

Honorary designations and commemorations
The Lyle H. Fulton Memorial Bridge in Nashville is named for a political candidate from Nashville who received the Democratic nomination for the Tennessee Senate in 1954, but died of cancer before the general election. Fulton's brother Richard, who later became Mayor of Nashville, was subsequently seated in his place. The bridge was dedicated in honor of Fulton on July 9, 1971. In addition, a number of short sections, interchanges, and bridges along the route are named in honor of state troopers and other law enforcement personnel killed in the line of duty, as well as local politicians and other prominent citizens.

In November 1998, the state commemorated the 40th anniversary of the completion of the first stretch of I-65 in Tennessee. On June 29, 2006, a historical marker celebrating the opening of this section as the first section of Interstate Highway was dedicated at the northbound Tennessee Welcome Center near Ardmore as part of the celebration of the 50th anniversary of the establishment of the Interstate Highway System. As part of the celebration, TDOT also produced a postcard with an aerial photograph of this section taken around the time of its completion.