The game received critical acclaim for its precise controls, voice acting, multiplayer modes, and replay value through the use of branching gameplay paths.

Most of the game takes place in "Corridor Mode", which forces Fox's vehicle down an on-rails path straight forward through the environment.

[3] These include silver and gold rings that refill the vehicle's shields, weapon upgrades, wing repairs, extra lives, and Nova bombs.

[4] All of the game's possible routes start at Corneria, eventually putting the player in contact with the Star Wolf Team, and end at Venom in a confrontation with Andross.

To add replay challenge, the game also features awardable medals, which are earned by accomplishing a mission with all wingmen intact and having achieved a certain hit total.

[4] Obtaining medals unlocks bonus features, such as new multiplayer vehicles, cosmetic changes to Fox in single player, and additional game settings such as "Expert Mode".

The player can use the fighter's boost meter to perform special techniques to avoid collisions, change direction, and gain tactical advantages in combat.

[4] At first, users can only play using the Arwing fighter, but by earning certain medals in the main campaign, players can unlock the Landmaster tank and fight on foot as one of the four members of Star Fox equipped with a bazooka.

The team consists of: Star Fox receives instructions and support from General Pepper, a bloodhound and leader of the Cornerian militia.

[7] Pepper hires the Star Fox team (including James McCloud, Peppy Hare, and Pigma Dengar) to investigate.

[13] Following the game's credits sequence, the player's final score is presented as a bill Pepper receives from Star Fox for their services.

By 1995, Miyamoto and team had largely finished development of Star Fox 2 before realizing that its release would require the upgraded Super FX 2 chip, which would increase the cost of the game.

[14] Furthermore, newly launched competitor consoles, namely the Sega Saturn and the Sony PlayStation, possessed processing power and graphics capabilities that dwarfed those of the SNES, making Star Fox 2 appear obsolete.

Around this time, Star Fox 64's development reportedly began with a series of experiments by character designer Takaya Imamura and programmer Kazuaki Morita.

As this was Morita's first attempt at learning 3D, he began with inputting his own data and placing objects like cubes on a course, and then launched basic-looking Arwings; this prototype was affectionately named "Star Box".

[16][17] Imamura and Morita continued their experiments for six months, becoming attached to it and wanting to realize it as a commercial product, while the higher-ups at Nintendo were reportedly not enthusiastic about the project and were even waiting for the two to give up on it.

[17] At some point in development, it was decided to include extra NPC characters such as Bill and Katt as a way to enhance the experience based on player interactions, to make their choices in the branching paths feel like they mattered.

[17] With the underlying gameplay largely complete early in development, Miyamoto and the team focused the majority of their efforts on graphics, audio and dialogue, and enemy AI, seeking to harness the Nintendo 64's processing power.

[19] In writing dialogue for the game's characters, the developers sought to invoke traditional historical dramas, adding more conventional lines such as "I've been waiting for you, Star Fox" and "You're becoming more like your father".

[24] This early version of the game showcased only the first level (Corneria) and featured a minimalistic HUD, showing only a crude meter reflecting the player's shield gauge.

Nintendo released further beta footage of the game on December 6, 1996, that showed subsequent levels, an improved HUD, and a short multiplayer segment.

[25] As the game approached launch, Nintendo became concerned that the title "Star Fox" could be considered too similar to the name of the German company "StarVox".

[3][6][41][44] However, Crispin Boyer of Electronic Gaming Monthly (EGM) considered them a waste, contending that the split screen display made targets too small to pinpoint.

[3] EGM gave it their "Game of the Month" award, with Dan Hsu calling it "a shooting fan's dream come true" and Shawn Smith "almost as good as Mario 64".

[6] The GameSpot review of the Wii Virtual Console version bestows a (7.6/10), praising its simple, enjoyable shooting gameplay, and much voice acting.

[51] In 1997 EGM ranked it the 39th best console video game of all time, citing its amazing visuals, huge amount of voice acting, and the deep challenge of earning medals on all stages and completing expert mode.