The blaze ripped through the famous clubhouse on Thursday, destroying the large wooden structure in the township of Bloomfield, Michigan that had stood since 1922.
Officials confirmed that no-one had been injured and they are unclear at this stage how the fire began.
Plenty of priceless golf memorabilia is said to have been lost, though staff and firefighters bravely battled to save as much as they could.
“We have lost our iconic clubhouse,” club president Rick Palmer said.
Oakland Hills was established in 1916 and contains two courses – South and North – both designed by Donald Ross.
It played host to the 2004 Ryder Cup, when a European team led by Bernhard Langer thrashed Hal Sutton’s USA by 181⁄2 to 91⁄2 points.
The venue has also hosted the US Open six times as well as three US PGA Championships, with Europe’s 2021 Ryder Cup captain Pádraig Harrington emerging victorious in the latter in 2008.
Australia’s Curtis Luck also won the US Amateur title there in 2017. In January, it was announced that Oakland Hills would host the US Women’s Open in both 2031 and 2042.