@seamus and @Nilav - We’re definitely sad to hear that you’re having similar-sounding issues. VirtualBox does create these network routing options in both environments but what you’re describing is pretty atypical for most folks.
It also sounds like the problem that @Nilav is having is a bit more flip a switch and it doesn’t work, while @seamus, yours is a little more nuanced, sometimes happening after a long period of time.
@seamus, since it sounds like you’re still using Local, the next time you have an issue with the network showing connected but not working, would you open up the Network preferences on your mac and check the IP address and DNS servers being used at the time? Additionally, check to see if you can renew the DHCP address on the connection that is not working:
What is the actual error you get in a browser when things aren’t working? Can you send a screenshot?
Has updating to the latest version of Local (3.3) made any difference?
Chances are, Ben is right that VirtualBox could be interfering but we’d like to help troubleshoot it some more if you’re up for it!