Star Fox 64's development didn't actually begin with the intention of creating a new Star Fox game; rather, it began with a series of experiments by character designer Takaya Imamura and programmer Kazuaki Morita. As Morita was new to 3D programming, creating something entirely new was difficult, and to make matters worse, they didn't have the final N64 hardware itself to work with, instead having to utilize a bulky dev computer and a modified SNES controller without analog sticks, as those were all being used by the Super Mario 64 development team, which were clearly given far more priority. The pair decided to begin development by porting the original Star Fox, which they thought would be better for easing into 3D. 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".

Star Fox 64's development wouldn't be given the full greenlight until the project was displayed at Space World 1995, as the higher ups within Nintendo were not actually keen on the concept and were even waiting for Imamura and Morita to eventually give up on their experiments. It was because of their dedication and perseverance to get the game off the ground that led to Star Fox 64 beginning full production as an actual video game after it was shown off at Space World, with Shigeru Miyamoto and other Nintendo staff such as director Takao Shimizu slowly coming on board afterwards.