The relationship between boss and board has become increasingly strained with the budget available for next season central to that tension.
Hughes' side won the Scottish Cup in 2015, their first major honour securing a maiden European campaign.
But the 51-year-old has become frustrated at the loss of key talent.
Striker Billy McKay was sold midway through last season and defender Graeme Shinnie and midfielder Marley Watkins later left as free agents.
And, most recently, forward Miles Storey, who spent this season on loan at Inverness from Swindon Town and scored 13 goals, has agreed to join Caley Thistle's Scottish Premiership rivals Aberdeen in July.
Earlier this season Hughes, who won Scotland's two main manager of the year awards last term, admitted his disappointment at not being allowed to talk to Dundee United when they made an approach following the sacking of Jackie McNamara.
An increasingly public difference of opinion over resources has emerged with Inverness stating next season's budget was agreed some time ago and reflected the initial outlay of last term.
That budget was added to as a result of significant injury problems but Hughes suggested finishing seventh in the league this season would increase available resources.
The club have retained a number of their current squad beyond this season but await the conclusion of negotiations with several first-team players.
Hughes took over from Terry Butcher at Inverness in late 2013, having previously managed Falkirk, Hibernian and Livingston.
As well as last season's trophy win and third-placed finish in the Premiership, Hughes also led the Highlanders to the 2014 Scottish League Cup final, where they lost on penalties to Aberdeen.
His playing career, as a defender, took in spells at both Falkirk and Hibs as well as Swansea and Celtic.
John Hughes and Inverness Caledonian Thistle are negotiating the detail of a package that will confirm the manager's departure from the club.