It will add more than 100 titles to Steam's online store and streaming service, including The Hunger Games, Twilight, and Saw franchises.
The full range is available to US users initially, with European customers having access to a small selection.
Lionsgate said availability would increase during a global rollout.
Steam, which is owned by game developer Valve, is the most popular digital games retailer, with more than 125 million users. The platform sells games through direct download, with extra gaming features like a friends' list and voice communication, built into the client.
It's not the first time Steam has released video through its store. Game trailers and advertisements have been available for years, and it previously released gaming-related documentaries Free to Play and Indie Game: The Movie.
It also struck a deal to sell the Mad Max film franchise to coincide with the release of the video game of the same name last year.
The deal with Lionsgate, however, is the first large-scale agreement with a major production company. A spokesperson for Valve said Lionsgate's blockbuster franchises represent the type of entertainment it hopes will drive the continued expansion of their content catalogue.
On launch, the worldwide selection is limited to 11 older titles, priced between Â£3.49 - Â£5.59 for a 48-hour rental - in line with other online rental prices for new releases. Unlike some of its competitors, however, Steam operates on almost any computer platform - including Linux and Mac - but does not yet offer its streaming service to mobile apps.
"Valve has a track record of diversifying beyond games with its Steam platform by selling other forms of software and as a company is willing to test out various technologies and commercial models to see what works," said Piers Harding-Rolls, head of games research at IHS Technology.
"Steam also offers a global distribution platform with users in all major markets and, for now, very little video content competition.  It also aligns with Valve's move into virtual reality with Steam VR, where platforms are taking advantage of 2D video content which is being consumed through VR headsets.
"I think this is a smart move from Lionsgate and could deliver a decent incremental revenue stream from its catalogue. "
Steam, the digital gaming platform, has started offering Hollywood film rentals to users after signing a deal with production studio Lionsgate.