Blackpool F.C.
On 3 April 1999 Oyston took over as chairman of Blackpool F.C, becoming the third member of the Oyston family to occupy the role, after his father, Owen, and mother, Vicki, from whom he inherited the role. Initially he took over the role of Managing Director, following the resignation of both the previous Managing Director, Gill Bridge and Vicki Oyston, who had resigned as chairman following what was described as "an ugly 'Oyston Out' demonstration by fans at the stadium". Oyston had been handed control of the club by his father, who was, at the time, still serving a prison sentence for rape. Oyston stated that his mother had quit to give him a level playing field and let him run the club his way after his father had promised he would not seek to take over again upon his release.
In July 2005 he was elected onto the Football League Board of directors as a representative of League One, and in June 2006 was elected back onto the board.
In September 2006 after an undercover investigation into illicit payments in football on the BBC Panorama current affairs documentary series, Oyston claimed that he had been offered bungs by football agents, saying "I've been offered cash as a bribe to bring a player to the club and it's happened more than once. In one instance, someone wanted me to take a player on a higher salary than we would normally pay, so he offered me a certain amount of cash as a gift to get me to do it. I said no and it didn't take any time whatsoever to reach that decision. Since 1999 when I became chairman here, my managers have been offered bungs. We've missed out on a lot of footballers because of it and that is one of my biggest concerns. It is very disturbing and in the Premiership where there are huge, huge deals taking place, it is a major problem." The Football Association asked Oyston, and others who made similar claims, to name the agents concerned, saying that they had a duty to provide evidence.
On 26 January 2010, Oyston was elected to the Football League Board of Directors as a representative of the Championship in a ballot for the vacant position. but had to leave this post at the end of the season following Blackpool's promotion to the Premier League.
In August 2010, Oyston offered to stand down as chairman of the club, stating his belief that he has a different approach to the rest of the Premier League chairmen and the difficulties of dealing with top-flight players and their agents. Oyston said: "The offer (to stand down) is still open. I have told the board and, yes, I am very serious. Why? Because I'm not sure I have the right approach to be in this division. The more I speak to other people at other clubs, the more I realise I am a lone voice. There was some support for things I did and said in the Championship but there doesn't seem to be any in this division. Everyone else seems to subscribe to the way that business seems to be conducted and it is a way I find unacceptable, so we'll see."
He added about agents: "We are the ones who are the employers. We are the ones offering the terms and the contracts. It is up to us how we go about things. I don't think any deal should be about the agent. It should be about the player, and about giving the player a platform under a wonderful manager to perform on one of the best footballing stages in the world. Agents are sometimes denying their clients that chance."
On 18 August, he stood down as both chairman and director of the club with immediate effect, although he remained as Acting Chief Executive. The following day it was reported that Oyston was involved in a bankruptcy hearing. Lancaster Crown Court confirmed that a judge was considering bankruptcy papers involving Oyston. The order was annulled on 12 October. Oyston returned to the his role as chairman in 2011.
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