Channel 4 has struck a three-year exclusive deal with BT to become its partner for TV ad sales on BT Sport 1, BT Sport 2 and ESPN.
The broadcaster will explore product placement opportunities and will create an auction process for betting partners, offering live odds and split screen technology on live sport.
Channel 4 director of sales Jonathan Allan said: "We're delighted to be representing BT Sport and it is a real coup for us to be chosen as a commercial partner.
"Alongside the Channel 4 portfolio, UKTV, Box and PBS, the addition of BT's premium sports content gives us an unrivalled ability to target young and upmarket audiences.
"Together, we are looking forward to changing the game in the way we work with advertising partners and build upon our reputation for innovation and challenging the status quo."
As well as 38 Barclays Premier League matches, BT Sport has secured broadcasting rights for football games in Italy's Serie A, Ligue 1 in France, Brasileiro in Brazil and the USA's Major League soccer.
Its acquisition of ESPN's channels will allow BT to broadcast FA Cup, Scottish Premier League, Europa League and German Bundesliga games, while rugby fans will be able to view rugby union games from the Aviva Premiership.
Chief executive of BT Retail, Marc Watson, added: "The companies are a great fit and with Channel 4's sales experience and our channels, we look forward to growing our businesses together in what we expect to be a very successful, long term partnership."
BT's new position in sports broadcasting has led to tensions with Sky as the broadcasters compete for dominance, which has refused to run any advertising campaigns for BT's new services on its sports channels.