Richards joined the group in the 1980s and has been described as Keith Miller’s right-hand man for the last two decades.
A member of staff said: “Everybody’s very shocked because John was in the building this morning chatting with colleagues and now he’s suddenly gone.”
He will be replaced by Richard Hodsden, former CFO at Safestore, from Thursday.
In a statement to staff Keith Miller said: “John has worked with the group since 1987 and has left to pursue other opportunities.
“We thank him for his valuable contribution to the company over this period and we wish him well for the future.”
He was appointed to the board in 1994 as group finance director. Prior to this appointment he was a director of Miller Homes and Miller Developments.
The Miller Group completed a £160m refinancing deal in March 2012 with US investment giant Blackstone, which took a majority stake in the firm.
Since then the group has steadily invested in the house building and construction business, anticipating the recovery.