Using the AGA chipset, it was originally released in small quantities in 1994 with a 25 MHz Motorola 68040 CPU, and re-released in greater numbers by Escom in 1995, after Commodore's demise, along with a new variant which featured a 50 MHz Motorola 68060 CPU.

Having driver software for both interfaces in the 512 KB ROM meant that some other parts of AmigaOS had to be moved from the ROM, and thus the A4000T was the only machine to require the file workbench.library to be stored on disk (this has changed, though, with the introduction of AmigaOS 3.2 and Kickstart 3.2, which too require workbench.library (and icon.library) to be stored on disk).

Modularity was another unique aspect to the machine, with the CPU, audio, video, and input-output ports all on separate daughterboards.

The case itself was a re-purposed PC case which is evidenced by the presence of the Turbo button whose function in A4000T was to disable the internal speaker (as Amigas don't support the PC-specific speed reduction which was the button's original function).

A4000T motherboards were also sold separately for OEM use, an interesting example being HDI-1000, an ultrasound machine made by ACL (a company later acquired by Philips) which in addition to the A4000T motherboard used a custom-built 68060 accelerator, and custom software based on AmigaOS.