Joint book runner Credit Suisse said Nixon is selling 80m shares in the first major disposal of his stock since the website floated in 2007.
Nixon set up Moneysupermarket.com in 1999 following the success of an earlier mortgage sourcing company.
He will now adopt a backseat role, after stepping down as chief executive in 2008 and in April moving from executive deputy chairman to a non-executive position.
Following the sale Nixon will be subject to a nine-month "lock-up" during which he will be unable to sell any of his remaining shares in the company.
Chairman Gerald Corbett said: "Simon remains a major shareholder and will continue to play a key role on the board."
