The two areas, which are currently car parks on Lord Street and Parade Street, occupy more than three acres.
Subject to planning, it is hoped the development will include leisure facilities, a hotel, shops and offices.
Infrastructure Minister Phil Gawne said potential designs need to "set the standard for future development".
He added: "This is an opportunity to develop a prime area in Douglas fronting the inner harbour and marina and close to the main shopping streets."

Starting and ending at the Town Hall in the city centre, the route took in views of the Peak District and a climb up to the village of Ringinglow.
The event saw shorter routes for junior runners, with the main 13.1-mile event won by Steven Bayton and Sarah Lowery.
Among the runners were retired rugby league players Barrie McDermott and Keith Senior.
Lowery, the first woman to finish the circuit, said: "I had not done this race before so it's nice to do your local half marathon.
"There were loads of people in the crowd all the way round, even in the really remote parts of the course, so I really enjoyed the race."
Councillor Mary Lea, from Sheffield City Council, said: "Although the route is undoubtedly a challenging one, the view from the top of Ringinglow Road across the Peak District is surely one of the best rewards any weary runner could hope for.
"I would go as far as to say that Sheffield is surely the most picturesque of almost any city half marathon, when you consider the blend of the beautiful rural landscape and the vibrant city centre finish."

The Supreme Court's judgement follows an appeal against the High Court's rejection of ministers' arguments.
Theresa May says the government already has powers to invoke Article 50 of the Lisbon Treaty - starting Brexit talks - by the end of March.
But campaigners say Parliament must be consulted before she does so.
Labour has already said it will not vote against the government over invoking Article 50.

With all eyes on May's general election, Carwyn Jones condemned David Cameron's Conservatives as being even more extreme than Margaret Thatcher.
He said voters had a choice between "hope and despair".
Meanwhile Labour leader Ed Miliband has launched an attack on tax avoidance for damaging the "fabric of society".
He told the conference there would be a "root and branch" review of Her Majesty's Revenue and Customs if Labour won the election, claiming the UK's tax authority had one rule for the rich and another for the poor.
In his keynote speech on Saturday, Mr Jones hailed the Welsh government's record on jobs, investment and tuition fees as evidence of what a UK Labour government could achieve.
He said the Conservatives "denigrate" the NHS in order to dismantle it, and insisted Labour's record on health in Wales was better than that of the Westminster coalition running it in England.
Mr Jones also called for a more "tolerant" society which could debate immigration with "fairness and respect", and not let "right-wing, dog-whistling xenophobes drag us down to their level".
A Â£40m scheme with the aim of helping people set up 10,000 new businesses creating 17,000 jobs over the next five years was also announced.
Unusually for the first minister, this was a speech dominated by attacks on the Tories.
He recalled the days of his political awakening during the miners' strike and said the current cutbacks were more severe than those felt in the 1980s.
He even likened the so-called bedroom tax to the poll tax.
There was some policy but basically this was a speech that acknowledged that the next few weeks is not about his government, although the Conservatives have other ideas.
Just to pick up on one comment: he took a hard line on health boards, saying he won't apologise if they fail.
This is a change of tone and I'm told it's the result of deep frustration with Betsi Cadwaldr health board in particular over the way last week's decision to move to a midwifery-led maternity unit at Ysbyty Glan Clwyd was handled.
I think we can expect more of this tone in future, as Welsh government ministers become more open in their views of health boards if they feel there are problems.
The Manx government has invited developers to come forward with ideas to transform prominent quayside sites in Douglas.
[NEXT_CONCEPT]
Thousands of runners have tackled the third Yorkshire Half Marathon under blue skies in Sheffield.
[NEXT_CONCEPT]
The government will learn next Tuesday whether it has won its legal battle to get Brexit under way without the need for a vote by MPs.
[NEXT_CONCEPT]
Only Labour can stop the Tories from decimating public services, the first minister has told the Welsh Labour conference in Swansea.