Following Richard Boyle's rise to power, Windebank throws his support to the Earl of Cork. Although, Boyle (secretly) loathed Windebank for his ego and insufferable arrogance but realized that his influence in powerful circles made suffering him a necessity. Because of this, Windebank was assigned to the Tower at the benefit of keeping him out from underfoot constantly at the real center of power in Whitehall. As constable of the Tower, he was responsible in overseeing Wentworth, William Laud, and Oliver Cromwell's imprisonment.
Windebank was involved in seeking the capture of Anthony Leebrick and his men to add the fabricated evidences against Wentworth, in which he decidedly recommended that Leebrick and his men's escape was sufficient evidence itself especially from the murder of Endymion Porter. Windebank and the conspirators decided to quietly let the search for Leebrick lapse into dormancy. Oftentimes, Windebank established a near-long term quarrel to Boyle's closest ally Sir Paul Pindar.
In 1633, the embassy from the United States of Europe was held in the Tower. Windebank was forbidden by Richard Boyle from searching the USE Embassy's quarters and belongings despite Windebank's deep suspicions of the dangerous kind of possessions they have, as any provocation towards the embassy would further exacerbate England's relationship with the United States of Europe in the Ostend War. When Windebank petulantly pressed his concerns on simply releasing the embassy to avoid any further conflict with the USE, Boyle annoyingly responded that using the untouched embassy would provide a valuable peace broker between England and the USE. This decision gave the USE the opportunity to connect with Cromwell through hand-held radio, and eventually escape along with the prisoners and the Yeomen Warders in 1634 during a commando raid by Harry Lefferts.