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.

Committee chairwoman Bethan Jenkins said it would "better reflect Welsh life" and AMs were pleased it was being considered by the corporation.
AMs also called for an extra Â£30m to be spent each year on BBC English-language drama and broadcasting about Wales.
The BBC said plans for more spending would be announced "in due course".
The broadcaster has previously conceded aspects of Welsh life had not been "sufficiently captured" by its TV services in Wales.
During its inquiry into the state of the broadcast media industry in Wales, BBC Director General Lord Hall told the Culture, Welsh Language and Communications Committee that putting Wales-based news bulletins on Radio 1 and 2 was being discussed as part of a review.
Ms Jenkins said her committee believed "flagship stations such as Radio 1 and Radio 2 should carry Wales-specific opt-outs for their news programmes to better reflect Welsh life".
AMs were "pleased to hear" this was being seriously considered, she added.
The committee's report said there should be no more funding cuts for S4C until an independent review of the channel had been completed.
It also called on ITV Wales to take a more proactive approach to getting its programmes broadcast across the ITV network.
A BBC spokeswoman said: "We've said that improving how we portray and represent the different nations of the UK - including Wales - on our UK-wide services is a priority for the new Charter period.
"As part of this we've committed to spending more on English-language television programming in Wales and will set out the proposals in due course."

Police made the discovery in the River Mersey in Chorlton, close to Darley Avenue and Barlow Moor Road, at about 09:45 GMT.
Officers were working to identify the victim and inform her family.
The death is not being treated as suspicious and police believe the woman may have suffered medical complications.

Second quarter operating profit rose nearly 5% to 3.49bn euros (Â£2.47bn).
But it listed a raft of potential problems, including "fierce competition, interest rate and exchange rate volatility, and fluctuations in raw materials prices".
The results come one day after news VW had overtaken Toyota to become the world's biggest vehicle maker.
But VW noted that robust growth in the global economy lost momentum in the first half 2015 and it said it expected the same level of growth for this year as in 2014.
VW cited risks to global financial markets resulting from "the strained debt situation of many countries".
It expects the strongest growth to come from Asian emerging economies, with moderate rates of expansion from major industrialised nations.
The company's shares are down more than 2% in Frankfurt.
The man in charge of delivering a major part of Bristol's MetroBus network has resigned from his role.
[NEXT_CONCEPT]
Welsh listeners to BBC Radio 1 and 2 should hear news bulletins about Wales at certain times of the day, according to the assembly's culture committee.
[NEXT_CONCEPT]
The body of an elderly woman has been found in a river in Manchester.
[NEXT_CONCEPT]
The German carmaker Volkswagen reported a rise in its quarterly profit, but noted slowing demand in key markets.