Nearly every piece of White House communication receives her input or approval.
Former press secretary to Vice-President Dick Cheney Juleanna Glover Weiss said: 'She's the chief traffic controller. She's one of only a few people in the White House who, when they said, "the President will be fine with that", you could take it to the bank.'
The President said Hughes would continue to advise him informally from Texas, where she plans to return with her family.
But White House veterans were quick to stress the challenges of advising from afar.
'You cannot impact in a real way the day-to-day workings of the White House, or the communications of the White House, unless you're at the White House,' said Joe Lockhart, former press secretary to president Clinton.
Glover Weiss agreed Hughes's absence would create 'a large vacuum', but added the post 'will be filled by the personalities that exist there now'.
Bush's PR team includes director of comms Dan Bartlett, press secretary Ari Fleischer, deputy director of comms Jim Wilkinson and deputy press secretaries Claire Buchanan and Scott McClellan.
'This is a President who is a very conservative person, both personally and politically,' said Lockhart.
'Hughes has been able to soften some of the right-wing policies and make them more tailored to the mainstream.'
Hughes has yet to publicly announce her career plans.