The Atari ST was part of the 16/32 bit generation of home computers, based on the Motorola 68000 CPU, with 512 KB RAM or more and 3½ "double-sided diskettes with dual density for storage (nominal 720 KB). It was comparable to other contemporary machines that used the Motorola 68000, the Apple Macintosh and the Commodore Amiga. While the Macintosh was the first widely available computer with a graphical user interface (GUI), it was limited to a monochromatic display on a smaller built-in In monitor. Amiga's release by nearly two months, the Atari ST was the first computer to feature a fully mapped color GUI, with a version of Digital Research's GEM released in February. It was also the first home computer with integrated MIDI -support.

Atari later improved the basic design in 1986 with the 1040STF (also written STF) in 1989. The machine was generally similar to the earlier 520ST, but moved the power supply and a double-sided floppy drive to the back of the computer's case, rather than being external. This added to the size of the machine, but reduced cable clutter in the back. The 1040 came with 1 MB of RAM and the same design was also used for the new 512 KB 520STFM, which replaced the earlier models on the market. The early 'STF' machines lacked the 'M' modulator allowing a TV to be used and only worked with a monitor.

The 1040ST was the first personal computer to ship with a 1MB base RAM configuration, and when the US list price was lowered to $ 999, it became the first computer to break the $ 1000 / megabyte price barrier and stood on the cover of BYTE. However, the ST generally remained the same internally for most of its multi-year life. The choice of model numbers is inherited from the model numbers of the XE series of the Atari 8-bit computers. A limited number of 1040STFs ship with a single-sided floppy drive.