Costikyan's notable works include

• Toon
• The Roleplaying Game (Origins Award Winner for Best Role-playing Rules of 1987)
• Pax Britannica (Charles S. Roberts Award Winner for Best Pre-20th Century Game of 1985)
• Paranoia (Origins Award Winner for Best Roleplaying Rules of 1984)
• The Creature That Ate Sheboygan (Charles S. Roberts Award Winner for Best Fantasy or Science Fiction Game of 1979)
• MadMaze
• The Roleplaying Game of Egregious and Repulsive Bloodshed

In addition, Costikyan is a widely-published author on the subject of game design and the role of games in culture. His essay, "I Have No Words and I Must Design"is widely read as a conceptual approach to framing game design.

Costikyan worked on game design for many years, including writing and consulting for Nokia. In September 2005, he left Nokia to join with Johnny Wilson, former editor of Computer Gaming World, in founding the startup indie game publisher Manifesto Games.He regularly contributes to Manifesto Games' website, and to their offshoot game review blog Play This Thing.

In the 1970s and 80s, Costikyan was a leading player of Slobbovia. His novel One Quest, Hold the Dragons includes several stories about crottled greeps, a Slobbovian meme.

In February 2009, Costikyan updated the rules and re-released his 1979 space combat game, Vector 3, under a Creative Commons license as a free PDF download.

Costikyan has written four novels. The first two were parodies of genre fantasy: Another Day, Another Dungeon (1990, ISBN 0-8125-0140-3) and its sequel One Quest, Hold the Dragons (1995, ISBN 0-8125-2269-9). By the Sword (1993, ISBN 0-312-85489-7) is another irreverent fantasy about a young barbarian who is forced by circumstances to make his way in the larger world; it was originally serialized on the Prodigy online service. His latest novel, First Contract (2000, ISBN 0-312-87396-4), depicts (with much dry humor) the vast sociological and economic changes that happen after aliens arrive on Earth, and one entrepreneur's efforts to survive and make a new start.

On March 7, 2007, Costikyan received the Game Developers Choice Awards Maverick Award. The award was given for his tireless efforts to create a viable channel for indie games.He was inducted into the Adventure Gaming Hall of Fame in 1999.