Francis entered St John's College, Oxford, in 1599, coming there under the influence of Laud.
After a few years' continental travel (1605 - 1608), he was employed for many years in minor public offices, and became clerk of the council.
The first earl of Portland, Francis, Lord Cottington, and Windebank formed an inner group in the council, and with their aid the king carried on various secret negotiations, especially with Spain.
In December 1634 Windebank was appointed to discuss with the papal agent Gregorio Panzani the possibility of a union between the Anglican and Roman Churches, and expressed the opinion that the Puritan opposition might be crippled by sending their leaders to the war in the Netherlands.
Windebank's efforts as treasury commissioner in 1635 to shield some of those guilty of corruption led to a breach with Archbishop Laud, and the next year he was for a time disgraced for issuing an order for the conveyance of Spanish money to pay the Spanish troops in the Netherlands.
In July 1638 he urged upon the king instant war with the Scots, and in 1640, when tumults were breaking out in England, he sent an appeal from the queen to the pope for mqney and men.
He was elected in March 1640 member of the Short Parliament for Oxford University, and he entered the Long Parliament in October as member for Corfe.
In Decemberthe House learnt that he had signed letters of grace to recusant priests and Jesuits, and summoned him to answer the charge, but with the king's connivance he fled to France. From Calais he wrote to the first Lord Hatton, defending his integrity, and affirming his belief that the church of England was the purest and nearest the primitive Church.
He remained in Paris until his death on the 16t of September 1646, shortly after he had been received into the Roman communion.
His was known by having Spanish and Roman Catholic sympathies.
Windebank married and had a large family. William Laud referred in 1630 to his "many sons". He had five at least, and four survived him.