The soccer world was left stunned on Tuesday when the United States, needing an away win or draw at bottom of the group Trinidad & Tobago to clinch one of the CONCACAF region's three automatic berths, suffered a humiliating 2-1 defeat.
The loss, coupled by wins from Panama and Honduras, meant that the United States have failed to reach the World Cup for the first time since 1986.
Head coach of the United States mens national team Bruce Arena during the FIFA World Cup Qualifier match between Trinidad and Tobago at the Ato Boldon Stadium on October 10, 2017 in Couva, Trinidad And Tobago.
"It is the greatest privilege for any coach to manage their country's national team, and as I leave that role today, I am honored and grateful to have had that opportunity twice in my career," Arena said in a statement released by the U.S. Soccer Federation.
"This certainly is a major setback for the senior men's national team program, and questions rightly should be asked about how we can improve.
"No doubt this process already has started and will continue so that U.S. Soccer can progress."
While Arena's announcement was sudden it was not unexpected, coming on the heels of what is being viewed as the worst calamity in U.S. soccer history.
It marked an inglorious end to Arena's second stint as manager of the national team.
"I want to thank Bruce for everything he has done for the game over a long period of time," said U.S. Soccer president Sunil Gulati during a conference call on Friday.
"It's unfortunate it ended on Tuesday the way it did but Bruce's record, both at the college level, at the professional level and with our national team programme has been extraordinary."
Considered by many to be American soccer's greatest coach of all time, Arena's previous tenure with the U.S. team included a run to the quarter-finals of the 2002 World Cup, the country's best result in the tournament.
Under his stewardship, the team shot to fourth from 19th in the FIFA world rankings but Arena's contract was not renewed after a first-round exit from the 2006 World Cup in Germany.
After the United States got the final round of qualifying in the North American and Caribbean region off to a bad start under Juergen Klinsmann losing the first two matches, the German was sacked and Arena brought in to rescue the Russia bid.
The 66-year-old seemed poised to accomplish that goal, needing only a draw against winless Trinidad and Tobago. However, two first half goals for the hosts sank Arena's men.
Defeat meant the U.S. also missed out on a playoff place, which would have pitted them against Australia next month for a spot in the finals.
"Obviously the biggest disappointment is for our fans," added Arena. "While this is a difficult time, I maintain a fierce belief that we are heading in the right direction.
"I don't know what the future holds for me but I can say this from the bottom of my heart: from the high of reaching the quarter-finals of the 2002 World Cup to the low of a few days ago; I have appreciated every minute of being a part of this program."
Prior to getting involved with the national team, Arena coached D.C. United to consecutive Major League Soccer Cup victories during the league's formative years.
He then captured three MLS titles during a remarkable four-season stretch with the Los Angeles Galaxy that came during one of the league's most competitive eras, before his return to the national side.