In his first TV interview, Nick Timothy suggested the PM and other ministers’ attitude meant the government has “not been prepared to take the steps” needed to make the most of Brexit.
And he warned the government’s mishandling of it risked “opening up space for a populist right wing party”.
His comments are in forthcoming BBC Two documentary Inside the Brexit Storm.
Mr Timothy, who is considered to have been one of Theresa May’s most influential advisers, said that the prime minister should have been clearer that different sides of the Tory Party would have to compromise much earlier on.
“One of the difficulties she’s had is that she’s tried to take every part of the party with her at different points.
“It would have been better to be clearer that not everybody in the party was going to get what they wanted.”
He added: “I think one of the reasons we are where we are is that many ministers, and I would include Theresa in this, struggle to see any economic upside to Brexit.
“They see it as a damage limitation exercise.
“If you see it in that way then inevitably you’re not going to be prepared to take the steps that would enable you to fully realise the economic opportunities of leaving.”
Mr Timothy, a Brexiteer, also said that many MPs write off Leave voters as “being racist, stupid or too old to have a stake in the future”, and warned that the government’s mishandling of Brexit risked “opening up space for a populist right wing party…this is one of the dangers of where we are right now”.
Mr Timothy, who many MPs consider to have been responsible for some of the mistakes of the 2017 general election campaign also said that Theresa May’s premiership had “not been bad, but unlucky”.
The interview is part of Inside the Brexit Storm, a behind-the-scenes programme following the BBC ‘s Laura Kuenssberg through the twists and turns of the Brexit process to be transmitted shortly.