Yes, X can use multiple drivers. Yours is a very similar setup as what I have. I have an NVIDIA 9800 GT with two monitors connected and an 2nd generation intel card with a single monitor.
I don't see any problems with your xorg.conf. I suspect that you will need to create an xorg.conf if only to tell X to use both nvidia and intel drivers. My xorg.conf looks very much like yours; I have three monitor and screen sections because the nvidia card has two monitors, but I'm pretty sure that X is ignoring those sections.
First, you will want to make sure that xinerama is disabled in xorg.conf (maybe not necessary).
xorg.conf:
Section "ServerFlags"
Option "xinerama" "off"
EndSection
When you do a xrandr --listproviders you should see both cards.
cody@IRIS> xrandr --listproviders
Providers: number : 2
Provider 0: id: 0x290 cap: 0x1, Source Output crtcs: 2 outputs: 5 associated providers: 1 name:NVIDIA-0
Provider 1: id: 0x48 cap: 0xb, Source Output, Sink Output, Sink Offload crtcs: 3 outputs: 6 associated providers: 1 name:Intel
If you don't see both cards, you probably are missing a driver. (But OP says console is using one and X is using the other, so they probably both work)
You should be able to use xrandr --setprovideroutputsource to add the Intel ports to the list shown by your xrandr | grep conn
In my case I use the names given by --listproviders:
xrandr --setprovideroutputsource Intel NVIDIA-0
If that doesn't add the Intel ports, it may be already connected in a way you can't see it. Disconnect it with:
xrandr --setprovideroutputsource Intel 0x0
Then try to connect it again:
xrandr --setprovideroutputsource Intel NVIDIA-0
All of the output ports should be shown now. And you should be able to add a display with the gnome display settings or with xrandr.
So when I finally got my intel display working, the nvidia displays decided that they needed to pan when I tried to move the mouse to the third display. It would now show the third monitor's content both on the third and second monitor. And the second's original content slid over to the first monitor with the first's content off-screen. It would slide back to normal if I tried to move the cursor over to the first monitor again.
I finally fixed that with another xrandr call:
xrandr --output DVI-I-2 --panning 3840x1200+1680+0/1920x1200+1680+0/0/0/0/0
This call requires knowledge of the physical screen geometry and logical layout. I have a 1680x1050 monitor, a 1920x1200, and a 1920x1080. They are in that order from left-to-right. The right most is connected to the intel card.
This call is setting the panning region on the middle monitor. --output DVI-I-2 happens to be the port connected to my middle monitor.
The first four numbers set the panning region to the total of the middle and right screens. 3840x1200 as width and height and +1680+0 to offset the region to start at top-left on the middle monitor. (Apparently [0,0] is at the top-left of the left monitor)
The next 4 numbers are the cursor tracking region. I set this to only track the cursor on the middle screen. This way when the cursor leaves this screen, it doesn't try to shift the image to follow the cursor.
The last 4 numbers define a border around the panning region. I'm just using the default values here.
Versions of related software I was using:
xorg-server-1.17.4
gnome-3.18.0
xrandr-1.4.3
Ok, I finally fixed this by removing the closed-source proprietary driver, and using the open source Radeon driver. See https://help.ubuntu.com/community/RadeonDriver
The open source driver fully supports my ATI card
CEDAR Radeon HD 5430/5450/6330/6350/6370
To install the open source driver it is enough to fully remove the closed-source one (more details at https://wiki.ubuntu.com/X/Troubleshooting/VideoDriverDetection#Problem:_Need_to_purge_-fglrx). This is what I used:
sudo apt-get remove --purge fglrx*
sudo apt-get remove --purge xserver-xorg-video-ati xserver-xorg-video-radeon
sudo apt-get install xserver-xorg-video-ati
sudo apt-get install --reinstall libgl1-mesa-glx libgl1-mesa-dri xserver-xorg-core
sudo dpkg-reconfigure xserver-xorg
sudo shutdown -r now
After restart both laptop screen and my external monitor screen worked. To set the resolution for the two monitors I used arandr tool.
To check all is ok:
sudo lshw -c video
should show ... configuration: driver=radeon latency=0
Hope this will be of help.
Best Answer
Timo Aaltonen has fixed this issue! Update your xorg-server. Thank you.