Comment 7 for bug 813343

More info. So normally I had the minimal xorg configuration, and would just use twinview when plugging in an external monitor.

I switched it to this:

# nvidia-settings: X configuration file generated by nvidia-settings
# nvidia-settings: version 280.13 (buildd@yellow) Fri Aug 5 12:31:28 UTC 2011

Section "ServerLayout"
    Identifier "Layout0"
    Screen 0 "Screen0" 0 0
    InputDevice "Keyboard0" "CoreKeyboard"
    InputDevice "Mouse0" "CorePointer"
    Option "Xinerama" "0"
EndSection

Section "Files"
EndSection

Section "InputDevice"
    # generated from default
    Identifier "Mouse0"
    Driver "mouse"
    Option "Protocol" "auto"
    Option "Device" "/dev/psaux"
    Option "Emulate3Buttons" "no"
    Option "ZAxisMapping" "4 5"
EndSection

Section "InputDevice"
    # generated from default
    Identifier "Keyboard0"
    Driver "kbd"
EndSection

Section "Monitor"
    # HorizSync source: edid, VertRefresh source: edid
    Identifier "Monitor0"
    VendorName "Unknown"
    ModelName "Apple"
    HorizSync 30.0 - 75.0
    VertRefresh 60.0
    Option "DPMS"
EndSection

Section "Device"
    Identifier "Device0"
    Driver "nvidia"
    VendorName "NVIDIA Corporation"
    BoardName "GeForce 9600M GT"
EndSection

Section "Screen"
    Identifier "Screen0"
    Device "Device0"
    Monitor "Monitor0"
    DefaultDepth 24
    Option "TwinView" "1"
    Option "metamodes" "DFP-0: nvidia-auto-select +0+0, DFP-1: nvidia-auto-select +1440+0"
    SubSection "Display"
        Depth 24
    EndSubSection
EndSection

And on first boot/login, the monitor works fine. However, If I open up nvidia-settings and disable the external monitor, nvidia settings complains but no more windows are placed on it (the mouse can still traverse into it).

Upon re-adding the external monitor to TwinView, however, this effect happens again.. black area where mouse can traverse but no windows. Logging out / back in "fixes" this, but that means loss of my session.

So it seems that whatever method nvidia settings uses to re-configure displays isn't being honored by Unity.