United chairman Nick Merry, with whom Jim Smith arrived as a double act in March, 2006, hailed the Bald Eagle as the reason the club still existed.
But he said that at the age of 67 - having been in club management since 1969 - Smith was wise to finally call a day.
He said: "It was a professional decision coming in to take over and a professional decision that we have just made. We are and will stay true friends.
"I don't think it is sad. It was a decision that will benefit everyone.
"Pressure at 67 is not always a good thing. I am sure he will still enjoy watching games.
"It was inevitable that he would retire at some point.
"Obviously he would have liked to have gone with a couple of wins, but without him I doubt whether Oxford United Football Club would be here.
"That's not stretching the statement too much."
Despite the club toiling in mid-table, Mr Merry said it was not too late to push for promotion.
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