But following his death on Wednesday, his sons Avram and Joel will now be calling the shots.
And with an ageing squad and no European football next season, the door is open for the brothers to sell up.
Glazer, who died last night aged 85, bought the club in 2005 in a controversial £790m takeover, using a number of loans to meet the asking price.
Manchester United went from being the richest club in the world to being the club laden with the most debt.
Despite not naming himself on the board, Glazer oversaw Avram and Joel who ran the club as executive co-chairmen.
His four other children Kevin, Bryan, Edward and Darcie also hold places as directors on the board.
Yet the Glazer's 90% stake in club, which is split equally among all six, could be shifted if the right bid comes in.
The value of the club currently stands at around £2bn, But with no European football next season there will be no commercial and TV revenue and the sale price is likely to drop.
Outside of Manchester United, the Glazers have a number of companies and business prospects to attend to following their father's death.
Bryan, Joel and Edward are all co-owners of NFL team Tampa Bay Buccaneers, which their father bought in 1995 for £114m.
The property company First Allied Corporation, which Malcolm founded in 1984, is also split between the three and Kevin.
While another company, The Glazer Family Foundation, is run by Edward and Darcie.
A struggle to maintain the group of profitable businesses may lead to the Glazers selling Manchester United, particularly if the club continues to decline on and off the pitch.
Could the Red Knights be preparing a second stampede?
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