[4] Tunney won the 1970 United States Senate election in California, but was narrowly defeated for re-election in 1976 by Republican S. I. Hayakawa.

[1] Tunney joined the United States Air Force as a judge advocate and served until he was discharged as a captain in April 1963.

In 1964, Tunney was elected as a Democrat in the United States House of Representatives from California's 38th congressional district (Riverside and Imperial counties).

In July 1969, while serving as a congressman, Tunney was called to Hyannisport, Massachusetts by Senator Kennedy, a friend and former college roommate,[13] to assist in dealing with the death of Mary Jo Kopechne following the Chappaquiddick incident.

Murphy's staunch support for the Vietnam War hurt his campaign and as the general election approached, Tunney overtook him in the polls.

In the 1972 Democratic Party presidential primaries, John Tunney, described by New York Times as one of the best friends of Edward Kennedy, endorsed Edmund Muskie.

American covert and military support for pro-US rebels there suggested a return to the policies that had led up toward the highly unpopular Vietnam War.

The Senate had postponed passage of the annual defense budget because of concerns that the bill contained funds for covert operations against Soviet-backed Angolan rebels.

The CIA conducted highly classified briefings for senators, including Tunney, providing an accounting of where money was being spent.

It was at this time that Tunney introduced an amendment that would cut $33 million from the defense budget that was to be allocated to pro-US rebels for covert operations.

As a prominent Democratic politician in the populous and electorally pivotal state of California, Tunney was considered a potential "national leader in the making", but "instead he seemed mired in indecision about both the issues and his own future".

Jeremy Larner, a former speechwriter often hired by Democratic politicians, provided a fictionalized story of John Tunney in the 1972 film The Candidate.

[18] That fall, Tunney was defeated in his reelection bid by Republican S. I. Hayakawa, the former president of San Francisco State University, who had never held elected office.

On April 23, 1977, Tunney married Kathinka Osborne, a member of the 1964 Swedish Olympic ski team, with longtime friend Senator Kennedy serving as the best man.

[23] In February 2003, Tunney joined former Senate colleagues George McGovern and Fred Harris in opposing the Iraq War.

John and Kathinka Tunney lived primarily in Sun Valley, Idaho (with homes also in New York and Los Angeles).

[26] Writer Jeremy Larner and director Michael Ritchie reportedly based the 1972 film The Candidate, starring Robert Redford, on Tunney's successful Senate race in 1970.

[27] Following his narrow defeat in 1976, Tunney largely stayed out of politics and committed himself to environmental causes, including serving on the board of Living with Wolves, an organization dedicated to raising consciousness of the animals’ importance.