Sheriff, who is also head of news at Number 10, will take on the role within the next few weeks.
The move follows just over three years at Number 10, with Sheriff replacing current acting director of group comms Nick Court.
She pointed to the development of planned high-speed railway HS2 and aviation as among the top issues for the department during 2013.
‘I’ve had a very interesting time at number 10, and worked through the transition from the Gordon Brown Government to the coalition,’ said Sheriff.
‘But I am ready for a change and another challenge, and wanted to do a much more strategic comms role using a range of channels.’
Among previous roles, Sheriff spent time as head of news at the Ministry of Justice.
Following the failure of the West Coast rail line bidding process, an inquiry was told by DfT staff in November that the department had cut ‘too deep and too fast’ in a search for savings.
Earlier in 2012 PRWeek revealed that the budget for press officers was to rise from £980,000 in the financial year 2011/12, to £1.04m in the financial year 2012/13.