Chris Sane left South Gloucestershire Council days before it emerged the cost of building the North Fringe to Hengrove route had risen £4.6m since November.
Amid months of traffic delays, the construction bill is now £16m higher than forecast two years ago.
Mr Sane resigned on 30 June for "personal reasons", the council said.
"We can confirm that Chris Sane has now left South Gloucestershire Council, with effect from 30 June," a spokeswoman said.
"Alternative arrangements have been put in place to cover this role in the interim."
Earlier this week, a report to the council's cabinet authored by the now former head of transport revealed construction delays were behind the rising costs of the MetroBus route, which runs from Cribbs Causeway to the north of Bristol, through the city centre to Hengrove in south Bristol.
South Gloucestershire will need to spend an extra £9.8m above its original £30.5m contribution to the scheme to cover the increased costs.
The report recommended the extra cash is taken from the highways maintenance budget over the next 10 years.
Commuters have been enduring roadworks associated with the scheme in the city centre, on the M32 and various other locations in South Gloucestershire.
The man in charge of delivering a major part of Bristol's MetroBus network has resigned from his role.