With a few exceptions, the gameplay in Star Fox 64 3D is very similar to that of the original N64 version. The player controls Fox's Arwing fighter jet using the Circle Pad to steer, the shoulder buttons to bank left and right, and the four right-hand buttons to fire lasers and bombs, boost, and brake. The directional pad allows the player to perform somersaults and U-Turns, which can also be performed with combinations of other controls, and to zoom in and out from the Arwing in "All-Range Mode". The player can also enable "Gyro Controls", using the 3DS's internal gyroscope sensor to control the Arwing. Character dialogue, messages, and control information are displayed on the bottom screen.

The single-player campaign features two modes: "64 Mode", which replicates the original game's objectives and difficulty, and "3DS Mode", in which difficulty and objectives have been tuned and balanced to account for the 3D perspective and gyro controls. A third "Expert" mode can be unlocked during gameplay, adding the difficulty of the original game's expert setting. Each mode separately tracks the player's scores and medals.

Star Fox 64 3D also features a new multiplayer "Battle Mode", which allows players to play up to 4-player local multiplayer (via Download Play), or to battle against CPU opponents.^[8] During battles, each player's face can appear on opponents' screens in a live reaction feed from the console's internal camera.^[9]

This multiplayer mode is completely separate from the single-player game and does not offer any bonus content, whereas the Nintendo 64 version allowed players to unlock the "Landmaster" tank and "on-foot" modes after completing certain requirements in the campaign. It also does not support online play.^[9]

The game is set on a group of planets in the Lylat system. Ingenious scientist Andross, a native of the fourth planet Corneria, is driven to madness and nearly destroys the planet using biological weapons. For Andross' treason, General Pepper exiles the scientist to the remote planet Venom. Five years after Andross' exile, Pepper detects unknown activity on Venom.^[10] Pepper hires the Star Fox team (consisting of James McCloud, Peppy Hare, and Pigma Dengar) to investigate. Upon arriving, Pigma betrays the team, and as a result James ends up missing and is presumed dead, while Peppy barely escapes. Several years later, Andross again invades the Lylat system, causing Pepper to call on the new Star Fox team, led by James's son Fox McCloud, to battle Andross.

At the 2010 E3 conference, Nintendo announced a remake of Star Fox 64 for the Nintendo 3DS, entitled Star Fox 64 3D.^[11] There was a demo tested the same day at Nintendo E3 2010. The demonstration had controls and character dialogue displayed on the touch screen. Nintendo added a kind of control that makes use of Nintendo 3DS's gyroscope to control the Arwing in space.^[12] At E3 2011, Nintendo confirmed a multiplayer for up to four players via 3DS Download Play.

At the annual E3 event during the Nintendo Q&A session held in June 2011, Miyamoto jokingly stated that he warned the developers that if Star Fox 64 3D was not the best game in the series, or did not make a lot of money, the franchise would have to be discontinued.^[13]

In an interview with the Official Nintendo Magazine, the game's planner Yusuke Amano reveals the reason why online support for the game was not implemented, stating that "just making multiplayer parts of existing games playable online isn't enough to create a satisfying experience for users. The popular online games work in lots of things, so they play well online - and if we wanted to satisfy everyone who bought the game, the costs required for including online support would be vast". Amano also cited that there were other reasons, such as time limits in development, and the developers' increased focus towards the graphics, in an attempt to amplify the appeal of the Nintendo 3DS console. However, Amano also added he would not rule out the possibility of online play in a future Star Fox game.^[14]

Star Fox 64 3D has received positive reviews, with a Metacritic score of 81, based on 65 reviews. Most critics agreed that it remained enjoyable. Critics praised its gameplay, visuals, and upgrades, with acclaim for its attention to detail and full recreation of the original. Common complaints, though, include a lack of online multiplayer and that the game is too similar to the original, claiming new content should have been included.

In October 2015, the game was inducted into the Nintendo Selects range in Europe,^[34] indicating global sales of over 1 million units.^[35] This was followed by Australia in May 2016,^[36] and North America in February 2019.

• Official website (archived)