Denning joined TSR as a game designer in 1981, and was promoted a year later to Manager of Designers, before he moved to the book department. He then worked for two years managing the Pacesetter game company, and had a stint at Mayfair Games, before going freelance.

Denning wrote the third novel in TSRs "Avatar Trilogy", Waterdeep (1989), which he wrote under the house pseudonym Richard Awlinson, with Scott Ciencin; the book became a New York Times bestselling novel. The choice of the surname Awlinson was an inside joke which sounds like "all in one".

In October 1989 he rejoined TSR as a senior designer, co-creating the Dark Sun setting with Tim Brown and Mary Kirchoff. According to Denning, the three designers envisioned "a world for experienced DMs that would push the AD&D game to its limits and let people do things like play half-giants and thri-kreen and superstrong characters...in short, all the really neat stuff we wanted to do ourselves, but that everybody kept saying would ruin game balance." Denning felt in 1998 that Dark Sun "did what we wanted it to, and it has attracted a devoted following. When I go to conventions, it's still what people want to talk about. Talking Brom into being the lead artist early was very fortunate for us; he would sketch weird creatures and settings and equipment, and we’d work them into the game."

Denning returned to freelance writing again in 1991, writing the bestselling "Prism Pentad" for the Dark Sun setting (1991—93), and the Forgotten Realms "Twilight Giants" trilogy (1994—95). Denning also wrote the Planescape hardcover Pages of Pain (1996): "It had to be from the Lady of Pain’s viewpoint...which is something of a problem, since (as every Planescape player knows) she never speaks...and (this was the really good part) the reader must know less about her at the end of the book than he does at the beginning, and nobody knows anything about her at the beginning." Denning recalled that Pages of Pain "really made me rethink the way I approach stories, and for that reason alone it was worth writing. It also ended up being a much deeper book than I had ever written before, which I think was a result of the extreme approach I was forced to take. Those who have [read it] seem to think it's my best work. It was certainly the most challenging and...forgive the pun...'painful' to write." Denning continued the story told in Waterdeep's sequel, Prince of Lies (1993) by James Lowder, with the novel Crucible: The Trial of Cyric the Mad. Denning then authored another Forgotten Realms novel called Faces of Deception. Denning's other notable works are Dragonwall and The Parched Sea.

He is also the author of a number of Star Wars Expanded Universe novels. Including Invincible, the ninth and final book in the Legacy of the Force series, was released in May 2008. He also authored the third and sixth books in the series. He has also been the author for three books in the Fate of the Jedi series.

Troy was one of the founders of Pacesetter Ltd, a game company formed by a group of former TSR, Inc. executives.

Denning lives in Wisconsin with his wife Andria. He enjoys outdoor activities, and practices martial arts.