The Blues - who struggled financially last season - have been give a huge boost after the donation was rubber stamped.
Murphy has gifted the club the huge sum over the next three years. The majority of the money will be used for infrastructure improvements to help the fan-owned club's overall sustainability.
"This gives me a great opportunity to give something back to the city of Chester and to the football club that I care for so much," said Murphy, who has sponsored the club’s stadium through his company Exacta.
"I have lots of ideas to move the club forward positively and I can't wait to get started. There is much to do, but I am confident that together we can now start to write a new and far more positive chapter in the history of Chester FC."
City Fans United chairman David Harrington-Wright said: “I am so pleased for everyone that we have been given this opportunity.
“I know that Stuart is brimming with ideas and we are so grateful to him for this generous donation and for his skill, expertise and time that he will commit to help our club.
"This is a one-off chance for everyone at Chester Football Club. If we all pull together, we can really make it work."