Initially, the Saudi embassy in Washington had sought to down play rumours of his departure - growing frenetically over the last few days, saying merely that he was going on holiday.
But Saudi officials who wished to remain anonymous confirmed to reporters on Wednesday that Prince Bandar, 56, had actually tendered his resignation.
It is thought he is heading for a senior position back home, with the post of intelligence chief having been vacant for several months now.
Some experts are commenting that the timing could be crucial, coming in the light of King Fahd's failing health - he has been in hospital for several weeks with pneumonia - and Bandar (who's elderly father is defence minister) is positioning himself in a possible succession battle.
Prince Bandar who has served for 22 years - the longest diplomatic posting to the US capital by any foreign country, became Saudi ambassador to Washington in 1983, when Ronald Reagan was in the White House and has been close to every president, Republican and Democrat, since.
Saudi oil has played a critical role in both countries, with the Gulf Kingdom being the world largest oil exporter and major supplier of oil to the US.
Bandar, a former Saudi air force pilot, is known to have developed a special bond with the first President Bush, a man he said he greatly admired for coming to the aid of the oil kingdom in the first Gulf War when Iraq invaded neighbouring Kuwait, heighting tensions.
He became a frequent family visitor to Camp David, the presidential retreat, and befriended George W.
Close to Bush
His relationship with the current president was famously depicted in Michael Moore's Fahrenheit 9/11 documentary, and in some circles, his close affinity to Bush accorded him the nickname, "Bandar Bush".
A man known to be colourful, with a lifestyle to match, he was considered one of the most influential ambassadors to the US.
Saudi Arabia's monarch is ailing
Wheeling and dealing behind the scenes, he has played a central role in building the special relationship between Riyadh and Washington - a task that has become significantly harder since the 11 September 2001 attacks.
Bandar was besieged by US lawmakers' complaints that Saudi Arabia had done far too little to suppress Al Qaida - the group behind the 9/11 attacks, though the criticism has ebbed since the kingdom began a major crackdown following bombings in the Holy Kingdom, blamed on the group in 2003 and 2004.
Last year, during the US presidential campaign, controversy briefly flared over reports that Bandar had promised Bush to help keep oil prices as low as possible during the election year, to favour Bush's re-eelction standing. The White House denied any "secret deal".
If the ailing Saudi King Fahd were to die, it is expected that Crown Prince Abdullah, 81, the de-facto ruler since 1995, would become king and Prince Bandar's father, Prince Sultan, 77, would become crown prince.
But with the current leadership very elderly, Prince Bandar may be positioning himself for future developments in a post-Fahd era.
There has been no word on who would be his likely successor in Washington.