Can a MacBook Pro reliably wake a Cinema Display when both are sleeping? I use a MacBook Pro with a Cinema Display and every time when I wake the MacBook Pro, the cinema display wakes first and the MacBook Pro display seems to stay in a sleep mode until I press the Detect Displays button in Displays Preferences. The most annoying part is that I need to rearrange all open apps' windows every time I wake my Mac. 

Does anybody have any idea how to fix this problem?
You ask for a fix where one of your screens does not wake up. I have a fix for a similar problem as my second screen on my MacMini (server 2011) does not wake up. It's not pritty but it is a fix.

I noticed that the screen wakes up after you change the screens refresh rates, so I use cscreen to do this. After my computer wakes up I run the following script. There are multiple solutions to run scripts just after waking up your machine (like Scenario and Power Manager).

#!/bin/bash
# b.nelissen

# cscreen: http://www.pyehouse.com/cscreen/

# wake up screen when one of these two displays are found
if [ "$(cscreen -l | grep '2b1052d0\|3c0c07c2')" != "" ]; then
    echo "Display found"
    # Dell screen does not wake up, switch back and forth to wake her up
    cscreen -i 2b1052d0 -d 32 -x 1280 -y 1024 -r 60 # small dell screen
    cscreen -i 2b1052d0 -d 32 -x 1280 -y 1024 -r 75 # small dell screen
    cscreen -i 3c0c07c2 -d 32 -x 1920 -y 1200 # big compaq screen
fi

# exit


What it does in short


Check if the screen is connected (I switch screens between home and work)
Refresh rate for displayID '2b1052d0' first to 60 than to 75 (to wake up the screen)
Set the second screen to her normal settings.