Xinerama was initially developed by SGI, and was used in their IRIX operating system. SGI systems have supported multi-head graphics for a long while. It was then ported to XFree86, providing Xinerama support under Linux, FreeBSD, NetBSD, OpenBSD and Minix. From here it made it into the Xorg code base, but not before it was incorporated by HP, IBM and Sun. HP-UX 11i, AIX 5.3L and Solaris 10 include support for Xinerama. In the case of Solaris, it is supported both on x86 and SPARC.

The window manager needs to have Xinerama support in order to detect which sections of the virtual display are associated with which physical display. Without this, weird things will happen, such as windows maximizing across both monitors (rarely the right thing), or windows opening on the border between heads. XFCE, GNOME, KDE, Window Maker and several others support this. The versions of CDE distributed by Sun, HP, IBM and SGI also support it.