Released in 1995, WC4 was produced on the then-unheard-of budget of USD $12 million. The majority of this budget went to the shooting of its full motion video, which retained the previous game's cast and used real sets instead of bluescreen techniques. The game required 6 CD-ROMs, but was later re-released on DVD for special DVD-ROM kits. A single-sided DVD version simply repackaged the game's content, while a double-sided DVD edition re-encoded the video to MPEG2 DVD-quality. 
The first game set after the end of the Terran-Kilrathi War, WC4 depicted a galaxy in the midst of a chaotic transition, with human civilians, Kilrathi survivors and former soldiers on both sides attempting to restabilize their lives. The game includes a large number of branching conversations in which the player must choose what response his character, Christopher Blair, will give; the choice may affect the other person's attitude toward your character, the morale of the entire crew, the player's next assignment and even the game's ending. As the man giving the orders, Blair often gets to choose what ship he will fly, what missiles it will carry, and what wingman (or wingmen) he will take with him.
WC4 was also the first Wing Commander game to have "redshirt" wingmen, who had minimal character development and were not important to the plot (as opposed to the flight groups of the previous three games, which contained at most ten pilots with distinct personalities). These redshirts can be killed permanently in combat, while main-character pilots always eject unless their death is mandated by the game's plot.
A novelization, by William R. Forstchen and Ben Ohlander, was published on October 1, 1996.
The war between the Kilrathi Empire and the Terran Confederation has been over for several years. Confed is attempting to stabilize its economy and social structure, after the abrupt end to thirty-five years of war. The Kilrathi survivors, now led by Melek, retainer to the late Prince Thrakhath, are having even more trouble with the same problem, since so much of their racial and societal makeup revolves around hunting and killing. Tensions between the outer colonies and inner Confed worlds are higher than ever. And the Savior of the Confederation? Col. Christopher Blair, retired, is trying to eke out a living on a desert world as a farmer.
Salvation comes from Major Todd "Maniac" Marshall, who bears orders: Blair has been recalled to active military service by Admiral Geoffrey Tolwyn. The conflict between the Confederation and the Union of Border Worlds has deepened, most recently with a monstrous attack on an unarmed medical transport (detailed in the opening movie). This transport is destroyed by a wing of mysterious fighters equipped with a bizarre new anti-ship weapon that doesn't explode, but rather incinerates the target's contents, leaving only a burning shell behind. Maniac is able to relate very few details on the recall order, but Blair gets an eyeful within five minutes of taking the cockpit when the station he's heading to is attacked by an Avenger Border Worlds fighter. Border World claims that similar strikes have occurred on their ships are ignored. In two weeks, the Confederation's governing Assembly will vote on whether or not to declare war on the Border Worlds, with Tolwyn assigned to a fact-finding mission which will essentially decide the issue. To assist him, Tolwyn assigns Blair to the TCS Lexington under war buddy Captain William Eisen, with the task of unraveling these tensions and getting to the bottom of the story. Serving with Blair are Maniac, Lt. Winston "Vagabond" Chang, and Lt. Troy "Catscratch" Carter, a Kilrath-o-phobe who joined the military a couple of years too late.
Blair can find no concrete evidence, other than the fact that no one can positively identify the harassing ships. Further undermining his confidence, Tolwyn transfers a new officer to the Lex, Captain Hugh Paulson, who soon manages to have Eisen removed from command. Not long after, Paulson calls Blair and Chang in for a surprise mission briefing: Eisen has just defected to the Border Worlds and is fleeing in a shuttle, with Maniac piloting. Once in space, Vagabond announces that he is going to follow Eisen over, and the player must choose whether to defect or not. If he does not, Blair returns to the Lex to meet a new cadre of pilots brought in by Paulson: cold, efficient, extremely talented. The best, and coldest, is a man known only as "Seether." Blair flies with them for several missions before being confronted with a Border Worlds attack, led by Maniac, who gives Blair another chance to come over. Staying loyal to the Confederation leads to certain death, making it clear what series creator Chris Roberts expects the player to do. Blair and Maniac succeed in downing the Lex, though Paulson escapes in a shuttle. But his shuttle's pilot, Seether, knows that their commanding officer will only see failure in his actions, and executes Paulson with his trademark knife.
If Blair chooses to defect when Vagabond goes over, he arrives with Eisen, Maniac, Vagabond and Catscratch at the BWS Intrepid, an old Durango-class carrier that has recently suffered immense damage from a Confed attack. Much of the senior staff has been killed, including former skipper Captain Dominguez, and the two officers currently sharing the command are Colonels Jacob "Hawk" Manley and Tamara "Panther" Farnsworth, famed for their actions in the Astoria system during the war. Panther and Hawk bow to the Heart of the Tiger, giving him the post of Wing Commander for the Intrepid's flight group, and Eisen becomes her captain in the lack of any other Navy personnel. Other notable Intrepid natives include Chief Technician Robert "Pliers" Sykes, far older and less pretty than Rachel Coriolis but just as canny with the planes if Blair is friendly to him; Col. John "Gash" Dekker, head of the ship's contingent of Marines; and Communications Technician Velina Sosa, whom Catscratch quickly takes a shine to. Eisen also takes the time to confide the reasoning behind his defection: he's been in touch with connections back on Earth, and it seems that this nascent Confed-Border Worlds war is being encouraged by elements within Confed—including whoever sent Paulson. If he wanted the whole story, Eisen saw no choice but to defect.
Pliers comes up with a number of new inventions, such as a jury-rigged cloaking device and a "Manned Insertion Pod"—a torpedo-sized coffin that can be used to land ground troops. Blair takes two of them in against a communications station in the Orestes System, where Sosa and Chang collect valuable data on the conspiracy. Unfortunately, only Sosa makes it out alive, as Vagabond fights off the station's Marine defenders on foot and is killed by a parting shot. It is at this point that the two plot paths rejoin and the game proceeds identically for all players, inaugurated by a video sequence of the Vesuvius being launched and in which Tolwyn tells James "Paladin" Taggart, now a leading Confed Senator, that Blair has defected. Tolwyn is sure this means treachery; Taggart, who has faith in Blair, wonders if he might have had a good reason for it.
Blair catches a distress signal from the Kilrathi Melek and rescues his friend's convoy. Melek brings with him flight recorder data of the sleek black ships using their incineration weapon against a Kilrathi transport. Then Eisen leaves the Intrepid, intent on sneaking back in to Earth and uncovering whatever he can; he leaves Blair in command, with Border Worlds Vice Admiral Eugene Wilford as his immediate superior. The player's next challenge, in the Peleus System, involves a giant electronic warfare ship that is capable of jamming radar, targeting sensors and even shielding. Finally, the player is given a choice on what system to attend next: at Circe, Confed forces are attacking innocent Border Worlds civilians, but the Speradon System contains many of Confed's latest munitions and vehicles of war. Panther advocates the former, Hawk the latter. Blair's choice not only affects gameplay (new hardware if he chooses Speradon) but the game's ending. In the final mission in both systems, however, Catscratch is sent to capture a peculiar Confed satellite and gets into trouble; Blair must decide whether to rescue him. Besides the obvious loss of a wingman, Sosa is frosty to Blair should he abandon the rookie. Finally, the Intrepid catches wind of a secret Confed freighter sneaking through the area, and Blair is assigned to subdue it so that Dekker and his boys can capture it. Pliers, clambering aboard in the aftermath, discovers a squadron of sleek black fighters and a single example of their incendiary weapon, called "Dragons" and "Flash-Paks" respectively.
The next mission takes place in the Telamon System, which is under attack by... Some sort of plague. The vast majority of the colony has died, but a few survive, hale and untouched, evidently due to some sort of innate immunity; regardless, the death toll is atrocious. The survivors at the FT957 colony implicate sleek black ships in the destruction; supposedly, the visiting Dragons dropped canisters that undoubtedly contained a biological weapon. Blair traces the attacking Dragons to the Axius System, which he infiltrates. There he discovers a secret starbase, guarded by the TCS Vesuvius, and thousands of black-clad soldiers, led by Seether, who commands when the true leader isn't there. But, today, he is, and Seether respectfully steps aside for his commanding officer: Admiral Geoffrey Tolwyn. His "Black Lance" operation will bring order and chaos back to the human race; they are instigating a war between the Border Worlds and Confed as a form of backhanded evolution. The Gen-Select Bioweapon, recently tested at Telamon, is the next obvious step in the plan: a virus that kills off all but the most genetically superior. Blair, barely getting over his horror in time, is forced to fight his way out.
The Intrepid, pursued heavily by the Vesuvius and Tolwyn's Black Lance pilots, makes a run toward Earth. Since Tolwyn needs Congressional support to launch his war, it's obvious what he plans to do, and Blair needs to get there first and stop him. The Intrepid must bypass a major starbase in the Ella System, and the player is given the choice to sneak past it or Flash-Pak it—killing thousands of civilians in the process. Besides possibly altering the game's ending, this choice also determines whether Blair will have the Flash-Pak when it comes time to take out the Vesuvius, a job made slightly easier by the intervention of the TCS Mount St. Helens, sister ship to the Vesuvius and recently hijacked by Captain Eisen. Finally, Blair duels Seether one-on-one above Earth and then lands at the Congressional Building.
The game's final battle involves not weapons but words. Tolwyn, who has just been promoted to Space Marshal, is in the midst of his "report" on the Border Worlds' "warmongering" when Blair, a shabby figure in his dusty flight suit, slips in. If the player chooses to make a dramatic entrance, Paladin gives him the chance to speak. The player must then choose from an array of conversational choices, deciding how to best bait Tolwyn into revealing his true agenda and thus prevent a Terran civil war:
BLAIR: Space Marshal Tolwyn believes that our victory over the Kilrathi was a fluke, that we, as a race, need tinkering with, engineering! If a few billion die along the way—well, they weren't worthy, anyway! Why can't we be more like the Kilrathi—addicted to conflict, the only meaning of life being found in death?! Tell us all, Admiral! Is that the price of freedom?!
TOLWYN: Mankind was at his zenith when fighting the Kilrathi. Now our society is crumbling. We have no goals, no focus. We've grown complacent and confused. Who will protect us when the next race wishes to dominate us? Who can tell where that threat will come from and when? No. We must be prepared.
Progress only comes through struggle. Fighting keeps us fit! Conflict ensures our readiness and survival. The Kilrathi understood this. They endured for millions of years, and so will we if we continue fighting. If we continue to perfect our methods of killing—
Paladin cuts Tolwyn off at this point, and if the player has scored enough points against Tolwyn, the Senate votes against war. Tolwyn is then indicted and convicted for his actions; lacking an appeal, he hangs himself in his jail cell. (If the player made the wrong choices, the opposite happens: war is declared, and Blair is convicted of treason and executed.) Finally, the game's ending movie depends on whether the player agreed more frequently with Hawk or Panther: Blair will either be seen helping Panther train new pilots at the Academy, or using Black Lance assets to crush rebellions with Hawk at his side.
Forstchen and Ohlander made a number of significant deviations from the video game with their novelization, rewriting large swathes of background information. Changes include the following:
- In the opening sequence of the novel, Blair accidentally replays a holographic message from Rachel Coriolis, establishing why she left him.
- Catscratch and Vagabond are missing almost entirely; they do not defect with Blair and their fate after the loss of the Lexington is unknown. Sosa romances Blair instead of Catscratch, despite a few false starts in which Blair points out that he could be her grandfather (to which Sosa replies, "you'd have to have started early").
- Maniac serves as Blair's second-in-command and begins to grow into the role, developing maturity and no small amount of leadership skills. At the end of the novel he is given a long-overdue promotion to Lieutenant Colonel and assigned as Wing Commander aboard a light carrier. (Despite this, during Marshall's next appearance in Wing Commander Prophecy he is still a free-wheeling, irresponsible major; this inconsistency in plot and/or canon has not been resolved.)
- The Border Worlds' technology is totally rewritten, replacing the video game's Banshee, Vindicator and Avenger with Wing Commander II-era fighters.
- Tolwyn, though stripped of his rank and ultimately a suicide, is acknowledged by the novel's characters as something of a tragic hero, a man taking on the bitter and unwelcome job of ensuring humanity's survival at any cost—essentially reversing the moral of the video game by suggesting that the ends justify the means. The other difference is that Tolwyn's sentence is life imprisonment in the novel whereas it is execution in the game.
- Blair is known primarily as the "Heart of the Tiger," his Kilrathi warrior-name and the most famous title of the man who ended the war. (Pilots' call signs are often bestowed by friends or instructors, and this particular call sign allows Blair to use the considerable weight of his celebrity status as a weapon in combat.)
- Colonel Christopher "Maverick" Blair: the player character, played by Mark Hamill, returning to his roots as a farmer on a desert-bound world.
- Major Todd "Maniac" Marshall: the frenetic, irresponsible younger brother to Blair's more calm personality, played by Tom Wilson of Back to the Future fame. An inspired but undependable flyer, Maniac is the source of much of the humor in the game. His self-centered attitude ends most of his socializing options, creating a running joke in which he constantly checks his armpits for an odor problem.
- Lieutenant Winston "Vagabond" Chang: rarely found far from a deck of cards when off duty. He is older than Blair and has seen quite a bit of the galaxy. Though still a consummate survivor, he is killed at the Orestes listening post in 2673—just after losing at cards to Maniac for the first time. Played by François Chau.
- Lieutenant Troy "Catscratch" Carter: afflicted with a case of hero worship toward The Heart of the Tiger, Catscratch soon finds out that Blair is as human (or Kilrathi) as anyone else. He can be killed permanently during the Circe/Speradon missions. Played by Mark Dacascos in an early role.
- "Seether": real name unknown, this brown-haired, brown-eyed man is the finest of the Genetic Enhancement program, now known as the Black Lance. He stands as Blair's final combat challenge on his run to Earth. Played by Robert Rusler.
Border Worlds pilots
- Colonel Jacob "Hawk" Manley: a battle-hardened warrior, Hawk serves primarily as the voice of decisive, aggressive action. A fellow TCS Tiger's Claw veteran, he flew in the Battle of Earth and had 96 kills before Blair's Temblor run. Played by Chris Mulkey.
- Colonel Tamara "Panther" Farnsworth: a veteran of the Kilrathi War, she flew alongside Hawk in the Astoria System. She is known for a much more pacifistic approach, preferring stealth and trickery to a stand-up fight. Played by Elizabeth Barondes.
- Captain William Eisen: Jason Bernard plays the middle-aged captain of the Lexington. He was Captain of the TCS Victory, with Blair, Maniac, and Vagabond under his command at the end of the Kilrathi War, and the pilots remain very loyal to him.
- Admiral Geoffrey Tolwyn: played by Malcolm McDowell in a portrayal so celebrated that it has been retroactively incorporated onto all of Tolwyn's previous appearances. Wily, charismatic and not a bit unbalanced, he is still one of the finest and most respected admirals in the fleet.
- Brigadier General James "Paladin" Taggart: Blair's fellow Tiger's Claw survivor who has now turned to politics. He now serves as a senator in the Confederation Assembly. Played by John Rhys-Davies.
- Captain Hugh Paulson: another member of the GenSelect conspiracy, and briefly Captain of the Lexington. He is killed by Seether for failing to prevent Eisen from acting on his suspicions. Played by the late John Spencer.
Border Worlds personnel
- Chief Technician Robert "Pliers" Sykes: an old man—very old. Nonetheless, he loves his work and can be counted on for several improvements to the game's fighter craft, including jury-rigged cloaking devices and upgraded storage space on missile racks. Played by Richard Riehle.
- Lieutenant Velina Sosa: the friendly face seen by pilots departing and arriving at the Intrepid, Sosa is a pleasant young woman seemingly untouched by the war. Played by Holly Gagnier.
- Vice Admiral Eugene Wilford: a lifelong denizen of the Border Worlds, he fought with distinction in the Kilrathi war and returned to protect his beloved homelands afterwards. Played by Peter Jason.
- Lieutenant Colonel John "Gash" Dekker: he received his nickname as a trainee when he gave himself such a fierce paper cut on a foil packet of rations that he had to be medevac'd out. Despite these ignominous origins, he survived the Battle of Repleetah and escaped a Kilrathi POW camp, one of the few living men who can claim either feat. Played by Jeremy Roberts.
- Melek nar Kiranka: Thrakhath's retainer, the first Kilrathi to bow to the Heart of the Tiger. Now the nominal leader of the Kilrathi nation, he helps maintain peaceful relations between Kilrathi and Terrans. Voiced by Barry Dennen, played by Christopher Bergschneider in an animatronic costume.
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