David Cameron was given £200,000 by his mother in 2011 on top of the £300,000 his father left him after he died in 2010.
Details of his income and tax affairs, released by Downing Street, also show the Prime Minister earned £90,000 in rental income from his family home last year.
He also earned more than £3,000 on interest from his savings and sold shares worth a total of £72,000 when he became Prime Minister.
Analysis: What We’ve Learnt From PM’s Tax Disclosure
The tax documents show Mr Cameron had a taxable income of more than £200,000 in 2014-15 and paid almost £76,000 in tax.
They also show that when he first entered Downing Street in 2010 he took advantage of a £20,000 tax-free allowance, but stopped claiming it last year.
And they suggest that Mr Cameron earned enough to benefit from the reduction in the top rate of tax from 50p to 45p after George Osborne cut it in 2012.
The two payments of £100,000 each from the Prime Minister’s mother will only become liable to inheritance tax if she dies within seven years of the gifts, made in 2011.
It is therefore estimated that, assuming she is still alive in two years, Mr Cameron will save inheritance tax of between £70,000 and £80,000 which he would have paid if his father had left him £500,000.
Had Mr Cameron received the half a million pounds in one lump sum he would have been liable to pay the inheritance tax because it would have been over the tax threshold of £325,000.
Downing Street revealed that after the Prime Minister’s brother Alexander was left the family home in Berkshire, Mrs Cameron also gave money to his sisters as well as the Prime Minister “to balance it out”.
Earlier, speaking to Tory activists in London, Mr Cameron said he was publishing the information because he wants to be completely open and transparent about it.
“I will be the first Prime Minister, the first leader of a major political party, to do that and I think it is the right thing to do,” he said.
Chartered tax accountant Gurpreet Sandhu told The Social Magazine that although Mr Cameron must have known the shares were “potentially politically sensitive”, everything he has done has been above board.
“What it does show to me is that just before he became Prime Minister, he selectively sold the shares in the unit trust that his father effectively ran, so he probably realised it wasn’t wise as Prime Minister to have these shares in an offshore fund and he sold those,” he said.
“But he held on to the other shares he had and he sold those after he became Prime Minister, so what this tells me is that he knew this is potentially politically sensitive, but he’s done absolutely nothing wrong.”
As well as releasing details of the Prime Minister’s finances, Number 10 announced that a new taskforce is to investigate allegations of tax-dodging and money laundering linked to the Panama Papers data leak.
The unit, which is being set up with initial funding of up to £10m, will be led by HM Revenue and Customs and the National Crime Agency and involve specialists from the Serious Fraud Office and Financial Conduct Authority.
Announcing the move, Mr Cameron said: “The UK has been at the forefront of international action to tackle the global scourge of aggressive tax avoidance and evasion, and international corruption more broadly.
“There is clearly further to go and this taskforce will bring together the best of British expertise to deal with any wrongdoing relating to the Panama Papers.
“This world-class operation will report to the Chancellor and the Home Secretary on their strategy for taking action later this year, when we will update Parliament.”
The move was attacked by the shadow chancellor, John McDonnell, who said: “The Prime Minister must be challenged on this unacceptable proposal. Any inquiry must be fully independent and in public.
“Having this proposed taskforce reporting to the Chancellor and Home Secretary, who are members of a political party whose donors are implicated, is a non-runner. The Government’s inadequate plans will fail to win back the trust of the public.”