During the Cold War, the Tu-22M was operated by the VVS (Soviet Air Force) in a strategic bombing role, and by the AVMF (Aviatsiya Voyenno-Morskogo Flota, Soviet Naval Aviation) in a long-range maritime anti-shipping role.[4] During the 1970s, Tu-22M made a few simulated attack runs against U.S. Navy carrier battle groups. The bomber also made attempts to test Japan's air defense boundary on several occasions. On Good Friday night, 29 March 2013, two Tu-22M3 bombers made simulated attacks on Sweden. The Swedish air defense failed to respond.

The Tu-22M was first used in combat in Afghanistan from 1987 to 1989. Its usage was similar to the United States Air Force deployment of B-52 Stratofortress bombers in the Vietnam War, dropping large tonnages of conventional ordnance. The Russian Federation used the Tu-22M3 in combat in Chechnya during 1995, performing strikes near Grozny.

At the time of the dissolution of the Soviet Union, some 370 remained in CIS service. Production ended in 1993. The fleet strength was about 84 aircraft in 2008.

The Russian military acknowledged the loss of a Tu-22MR recon aircraft to Georgian air defences early in the 2008 South Ossetia war. One of its crew members was captured (Major Vyacheslav Malkov), two others were killed and the crew commander is missing in action as of August 2009.

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