Mac mini cannot use third monitor after OS upgrade

The symptoms you describe are quite specific, and they point away from cables, individual monitors, or a simple display preference problem.

The important clue is that the M4 Pro Mac mini recognizes whichever two displays are currently active, but will not maintain all three simultaneously. 

Since you previously had all three working with the same hardware, and the problem began with a macOS upgrade, I would first verify the Mac's supported display configuration and then reset the display configuration rather than deleting preference files blindly.

For an M4 Pro Mac mini, Apple officially supports up to three external displays when using the appropriate Thunderbolt/USB-C connections, so three displays are not inherently beyond the hardware's capability.

The first thing I would do is check System Settings >> General >> About >> System Report >> Graphics/Displays with all three monitors connected and powered on. If all three displays are listed there, even though only two are actually showing an image, that would be particularly useful because it would distinguish a display-detection problem from a display-output/configuration problem.

I would not start deleting .plist files or using Terminal commands. 

There is a safer diagnostic step: shut the Mac down completely, disconnect all three displays, start the Mac, log in, and then reconnect the displays one at a time, waiting several seconds between each connection. 

This can force macOS to rebuild its current display topology without manually deleting configuration files.

Also check System Settings >> Displays while all three are connected. 

Hold the Option (⌥) key; macOS may expose additional display-detection controls depending on the version. If the third display is detected but remains unavailable, that is more significant than simply not appearing.

One other thing I would specifically investigate is which USB-C/Thunderbolt ports the three displays are using. 

On the M4 Pro Mac mini, the exact supported combinations matter. Because you are using three USB-C/Thunderbolt connections rather than HDMI, I would verify that your particular combination of Studio Display + two U2725 displays is supported by Apple's current M4 Pro display specifications rather than assuming that three USB-C displays are interchangeable.

Given that this started after the OS upgrade, I would check whether macOS 27.0.1/Golden Gate actually changed the supported display configuration or contains a display-related regression before attempting any preference reset. 

That is something I would re-verify against Apple's current documentation and recent reports rather than guess.

Temporarily set both Dell U2725QE displays to 3840 × 2160 at 60 Hz. The U2725QE supports refresh rates up to 120 Hz, so this is a good way to rule out a refresh-rate or display-configuration issue without changing any system files. Dell UltraSharp U2725QE specifications

I would not delete preference files or use Terminal yet. 

The important clue here is that the same Mac mini successfully ran all three displays before the macOS upGrade, and each Dell works when the other one is switched off. 

That makes a bad cable or failed monitor less likely. 

The fact that macOS moves the picture from one Dell to the other when you switch them on and off also suggests that it is detecting the displays but  is not keeping all three active.

With all three connected, go to System Settings >> Displays and see whether macOS lists all three, including the one whose screen is currently blank. 

If all three appear there, we know the Mac is detecting them and can concentrate on why it would not activate all three simultaneously.

As a simple test, temporarily set both Dell U2725QE displays to 3840 × 2160 at 60 Hz. The U2725QE supports refresh rates up to 120 Hz, so this is a good way to rule out a refresh-rate or display-configuration issue without changing any system files. Dell UltraSharp U2725QE specifications

If that does not help, the next thing to check is the exact Mac mini model and how each display is connected. 

Apple's supported three-display configurations vary according to the Mac mini model, display resolution and refresh rate, and the connection being used. Apple: Connect displays to your Mac mini

If your particular setup is within Apple's specifications, then the fact that it worked before the upgrade becomes an important clue that  we are dealing with a macOS display-configuration problem rather than an inherent limitation of the Mac. 

In that situation, I would follow Apple's display troubleshooting steps before touching preference files or using Terminal. Apple: If your external display isn't detected or appears blurry

If you tell us what  >> About This Mac shows for the chip (for example, M4 or M4 Pro), which port and cable connect each of the three displays, and whether System Settings >> Displays shows all three when one is blank, we can narrow this down without resorting to trial-and-error changes to macOS.

Try the following script. It has worked for a few users at work

/bin/zsh <<'EOF'
setopt NULL_GLOB

backup="$HOME/Desktop/display-prefs-backup-$(date +%Y%m%d-%H%M%S)"
mkdir -p "$backup"

echo "Backing up display preference files to: $backup"

for f in /Library/Preferences/com.apple.windowserver*.plist; do
  sudo cp -p "$f" "$backup/" 2>/dev/null || true
done

for f in "$HOME"/Library/Preferences/ByHost/com.apple.windowserver*.plist \
         "$HOME"/Library/Preferences/ByHost/com.apple.preference.displays*.plist; do
  cp -p "$f" "$backup/" 2>/dev/null || true
done

echo "Removing display preference files..."
sudo rm -f /Library/Preferences/com.apple.windowserver*.plist
rm -f "$HOME"/Library/Preferences/ByHost/com.apple.windowserver*.plist
rm -f "$HOME"/Library/Preferences/ByHost/com.apple.preference.displays*.plist

killall cfprefsd 2>/dev/null || true

echo "Done. Rebooting now."
EOF

sudo shutdown -r now

What year model and sub model is your Mac mini...?

Identify your Mac mini model - Apple Support

Technically some of the base model Mac mini's only supported two or three displays.

One from the HDMI port and one or two from the TB/USB-C ports.

Connect a display to Mac mini - Apple Support

macOS updates have been known to render long cheap poorly made after-market display cables unusable.

Sadly the only way to prove that is to replace those with short high quality display cables.

Another option is to move and test one Dell to the HDMI port.

toucantoo wrote:

It's a Mac Mini from 2024 with the Apple M4 Pro Chip.

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Mac mini (2024) - Tech Specs - Apple Support

Apple M4 Pro chip

Simultaneously supports up to three displays:

• Up to three displays: Three displays with up to 6K resolution at 60Hz over Thunderbolt or HDMI
• Up to two displays: One display with up to 6K resolution at 60Hz over Thunderbolt and one display with up to 8K resolution at 60Hz or 4K resolution at 240Hz over Thunderbolt or HDMI

Thunderbolt 5 digital video output

• Support for native DisplayPort 2.1 output over USB‑C

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Also see: How many displays can be connected to Mac mini (2024) with M4 Pro chip - Apple Support