David Jones' career started with the indie game Menace, which he developed himself under the company name DMA Design and released in 1988. The game sold 15,000 copies and earned him £20,000, which he used to buy a car. DMA Design expanded and went on to make a second game, Blood Money, which Jones saw as a "further development" of the concept used in Menace. DMA created a third game in 1991, Lemmings, which was commercially and critically successful, resulting in awards including winning European Game of the Year twice. Over the next two years Lemmings sold over 2 million copies, making Jones, 25 years old at release and married with a child, wealthy and famous.
DMA Design created several more games over the next few years, but Jones spent time developing an idea for a fighting simulator set in a city; after the release of Syndicate Wars (1996), the company revised the concept to set it in a "living city" and cross it with a driving game, resulting in the successful and controversial Grand Theft Auto, which in turn sparked an entire franchise. In 2012 Jones revealed that much of the controversy surrounding Grand Theft Auto was engineered by their publicist. DMA Design was soon after acquired by Gremlin Interactive, starting a chain of purchases that resulting in the studio becoming Rockstar North. Jones stayed with the company through 1999 and Grand Theft Auto 2 before leaving.
In 2000 Jones founded and lead the Dundee studio of Rage Software, Rage Games (Scotland) Limited, where he developed the PC title Mobile Forces. Jones also co-founded Denki who developed Go Go Beckham for Rage.
In 2002 Jones founded Realtime Worlds, who developed Crackdown (2007) and APB: All Points Bulletin (2010).
In 2012 David Jones started work on ChronoBlade, a Facebook action-RPG game, with Stieg Hedlund as part of San Francisco-based development team nWay.
In 2012 he co-founded Cloudgine, a games development company focusing on cloud computing.Cloudgine.
In the same year Jones founded Reagent Games, serving as Creative Director, to lead the development of upcoming Microsoft XBOX ONE title Crackdown 3.
In December 2017, Cloudgine was acquired by Fortnite and Unreal Engine developer Epic Games; with this, Jones became Director, Cloud Strategy for Epic Games, and resigned from Reagent Games.