The player takes the role of a nameless pilot aboard the TCS Tiger's Claw, a Bengal-class Strike Carrier. The player gets to name the pilot and choose his call sign. The pilot (known in-production to Origin personnel as "Bluehair," after his most notable feature) quickly rises through the ranks of the flight wing, and (presuming the player performs ideally in the cockpit) eventually leads a strike on the Kilrathi High Command starbase in the Venice system. On the other hand, if the player does not perform optimally, missions become increasingly defensive in nature and eventually the Claw is forced to retreat. Of the two endings, the "winning" path is established as canon by the game's two expansion packs, as well as the sequel, Wing Commander II: Vengeance of the Kilrathi.

Wing Commander was originally titled Squadron, later renamed Wingleader. As development for Wing Commander came to a close, the EMM386 memory manager the game used would give an exception when the user exited the game. It would print out a message similar to "EMM386 Memory manager error..." with additional information. The team could not isolate and fix the error and they needed to ship it as soon as possible. As a work-around, Ken Demarest, a developer on the game, hex-edited the memory manager so it displayed a different message. Instead of the error message, it printed "Thank you for playing Wing Commander."

In August 2011 the long lost source code of Wing Commander I was handed to the fan-community by a former developer for the purpose of long-time preservation.

Wing Commander shipped with an instruction booklet styled as a shipboard magazine, Claw Marks. It provided tactical suggestions, statistics on fighters and weapons both Kilrathi and Terran, capsule biographies of notable pilots on both sides of the line, and general shipboard news (such as the discontinuation of the popular comic strip Hornet's Nest, due to the recent death of its artist, Lt. Larry "Tooner" Dibbles). Notable contributors to the Claw Marks magazine include Captain Aaron Allston, Major Warren Spector, and Col. Chris Roberts.

Wing Commander: The Secret Missions

Wing Commander: Secret Missions is an add-on campaign that requires the full game software to run, adding new missions, new ships, a new storyline, and an increase in difficulty. Unlike the original game, The Secret Missions does not feature a branching mission tree; every player plays the same missions in the same order. However, if the player does not the fulfill the mission requirements at any system, he immediately plays the two losing "retreat" missions that are not on the winning path. The Secret Missions was also released for the SNES as a stand-alone cartridge.

In the add-on's plot, the Tiger's Claw, on maneuvers in the Goddard System, receives an abortive distress call from Goddard colony. When the Claw arrives, though, nothing is left but wreckage and corpses; a quarter of a million colonists have been killed. Confed realizes that this is the work of a new Kilrathi weapon, the "Graviton weapon," which is able to increase the power of gravity by over a hundred times. Clever work by the Claw's crew and pilots allows them to capture a Kilrathi courier ship, which reveals that this weapon is mounted on an entirely new class of ship; CNC codenames it the Sivar-class dreadnought, after the Kilrathi god of war. Bluehair leads the strike against the Sivar and destroys it in the Vigrid system; for unexplained reasons, ships of that class and armament are never seen again.

Wing Commander: The Secret Missions 2: Crusade

The second expansion pack for Wing Commander, The Secret Missions 2 adds a new narrative, new ships, more difficult missions, and two new wingmen.

In the add-on's plot, the Tiger's Claw is in the Firekka System, whose native intelligent lifeforms — the bird-like Firekkans — are negotiating to join the Terran Confederation. Tensions are high, and will only get higher. There is an unusual Kilrathi presence in the area, including their upgraded Dralthi II and ships that have never been seen before: the Hhriss-class heavy fighter and the Snakeir-class heavy carrier. This presence develops into a massive battle group, and though the Firekkans sign the Articles of the Confederation, the outnumbered Terrans have no choice but to retreat. Adding to the mess, a Kilrathi lord, Ralgha nar Hhallas, defects, bringing his Fralthi-class cruiser, the Ras Nik'hra, and word of a rebellion against the Empire on the Kilrathi colony of Ghorah Khar. Finally, almost overlooked in all the chaos, Major Kien "Bossman" Chen is lost while flying on Jeannette Devereaux's wing; the nearby TCS Austin transfers over two pilots, Lieutenants Zachary "Jazz" Colson and Etienne "Doomsday" Montclair. All this happens in the first six missions of the game. The Kilrathi presence in the Firekka sector is eventually explained by an all-channels transmission from the Crown Prince of the Kilrathi Empire, Thrakhath nar Kiranka: Firekka has been chosen as the site of this year's Rite of Sivar, a religious festival that involves live sacrifices. Seeing the chance to strike a heady blow to Kilrathi morale, the Confederation assigns its Firekka-sector resources the task of disrupting the ceremony. The Dralthi medium fighters from the Ras Nik'hra are put to work on reconnaissance missions (conveniently, the Confederation Scimitar medium fighter is retired at the beginning of the expansion pack, opening a space in the database of Confederation fighters for the Dralthi), and Terran troops begin landing in secret. Between these, the Firekkans' warrior spirit and some of the Confederation's best pilots and tacticians, the Sivar ceremony is utterly wrecked and the Kilrathi forced to retreat, though they take a number of important Firekkans with them as hostages. Ralgha and the rebellion at Ghorah Khar, though promising, are taken over by Confed Intelligence and do not see mention until the first expansion pack for Wing Commander II. At the end of Crusade, Jeannette Devereaux is detailed off to the TCS Austin, where she will serve as Wing Commander.

Interested in the other half of the crusade, Mercedes Lackey and Ellen Guon penned the first Wing Commander novel, Wing Commander: Freedom Flight. It tells the Firekkan side of the story, from several points of view: Ralgha nar Hhallas, Ian "Hunter" St. John, James "Paladin" Taggart, and K'kai, a Firekkan flock leader.

Super Wing Commander

Super Wing Commander released in 1994 for 3DO was a drastic new look at the events of the original Wing Commander game with enhanced graphics and full speech. In 1995, it was also ported to Macintosh. The game also contained both Secret Missions and a special third campaign was also created between them (called "Secret Mission 1.5" by fans). That mission lead the Tiger's Claw to track down and destroy the shipyards responsible for creating the Sivar Dreadnought. Additional background elements rumors about stealth fighters and Admiral Tolwyn were added to improve the continuity with Wing Commander II.

Wing Commander I

In 1994, Wing Commander was retroactively renamed Wing Commander I in a bundled re-release together with Wing Commander II, in preparation for the release of Wing Commander III: Heart of the Tiger. The rebundled remakes do not contain and do not support the Secret Mission addons.

EA Replay

Electronic Arts ported the SNES version to the PlayStation Portable as part of EA Replay, released in the United States on November 14, 2006.

Dragon gave it 6 stars, out of a 5-star system, the Secret Missions Expansion Disk receiving 5 stars. In a review by Computer Gaming World, Wing Commander received the score of 10.91, the highest rating in the history of the magazine until 1992, when it was superseded by the game's own sequel, Wing Commander II. It also won Computer Gaming World's 1991 Overall Game of the Year award.

In 1996, Computer Gaming World ranked it as the seventh best PC video game of all time, also listing the game's Game Over funeral cutscene among the 15 best ways to die in computer gaming. In 2011, Maximum PC included it on the list 16 classic games that need to be remade today, stating: "Chris Roberts and Origin really nailed the space opera with this series, which blended fast action and a fairly engaging (if hokey) story. Way ahead of its time." In 2012, Time named Wing Commander one of the 100 greatest video games of all time, remembering its "unprecedented detail" of graphics and calling it "a revelation in 1990 for PC space-sim buffs looking for a little less Star Trek and a little more Star Wars from the genre."