Office

Destin, FL Office Spaces for Lease

Notify Me
List
Map
Miramar Beach, FL Shalimar, FL Fort Walton Beach, FL Niceville, FL Valparaiso, FL Mary Esther, FL Santa Rosa Beach, FL Navarre, FL
32 properties
Sort:
1012 Airport Rd, Destin, FL 32541
1012 Airport Rd, Destin, FL 32541

1012 Airport Rd, Destin, FL 32541

$129-$5,487/Mo
11-1,292 sqft

Office Spaces

View details
Office Space at Destin Commons
Updated: Nov 1, 2025
Office Space at Destin Commons

4300 Legendary Drive, Destin, FL 32541

$4,000/Mo
Premier location within Destin Commons, the Gulf Coast's leading open‑air center.
Move‑in ready professional office space featuring a reception area, three private offices, break room, and open collaborative area.
Ample parking just steps from the office.
24‑hour on‑site security ensures a safe work environment.
Flexible layouts available on both the first and second floors.
View details
Remodeled Office Condo Suite
Updated: Jul 1
Remodeled Office Condo Suite

1217 Airport Road #419, Destin, FL 32541

$2,733/Mo
1,312 sqft $25 SF/Yr
±1,312 SF commercial office condominium suite in a professional office setting
Built in 1999 and in a well‑maintained office condominium environment
Recently remodeled suite with a functional office layout
Tenant in place: regional staffing company; lease extends through May 2026
Located on Airport Road with easy access to US‑98 in Destin
View details
Turn Any Listing Into an Investment Snapshot Owner equity, real caprate, demand score for every listing. Go To Analytics Center
High-Visibility Retail and Office Space
High-Visibility Retail and Office Space

503 Harbor Boulevard 1, Destin, FL 32541

$6,700/Mo
7,000 sqft $11.49 SF/Yr

Flexible first- and second-floor suites offer strong street visibility and parking for retail or customer-facing services.

View details
Fully Renovated Retail/Office Space
Fully Renovated Retail/Office Space

4507 Furling Ln, Destin, FL 32541

$3,000/Mo
1,400 sqft $25.71 SF/Yr

Light, bright retail/office suite on the first floor of The Plaza, positioned along Highway 98 for strong daily exposure.

View details
Class A Office Suite
Class A Office Suite

982 Airport Road #A, Destin, FL 32541

$1,300/Mo
920 sqft $16.96 SF/Yr

Well-appointed office space in a three-building office complex, suited for professional tenants seeking a Class A setting.

View details
Destin Office Space For Lease
Destin Office Space For Lease

2 Industrial Park Lane #A6, Destin, FL 32541

$1,470/Mo
23,770 sqft $0.74 SF/Yr

Office space for lease in Destin, Florida.

View details
Destin Commons: Retail & Office
Destin Commons: Retail & Office

4008-4367 Legendary Drive, Destin, FL 32541

$27 SF/Yr
160,000 sqft $360,000/Mo

Premier retail, dining, entertainment, and office space on Emerald Coast.

View details
Professional Office Space Available
Professional Office Space Available

501 Harbor Boulevard #B, Destin, FL 32541

$1,350/Mo
9,400 sqft $1.72 SF/Yr

Office space in Norred Plaza on Highway 98/Harbor Blvd.

View details
Destin Office Space For Rent
Destin Office Space For Rent

151 Regions Way #2A, Destin, FL 32541

$2,232/Mo
1,102 sqft $24.30 SF/Yr

Office complex in central Destin, close to shopping and amenities.

View details
Destin Office Space For Rent
Destin Office Space For Rent

151 Regions Way #5A, Destin, FL 32541

$4,832/Mo
1,875 sqft $30.92 SF/Yr

Office space in central Destin, close to shopping and amenities.

View details
Destin Office Space For Rent
Destin Office Space For Rent

4458 Legendary Drive #230, Destin, FL 32541

$1,640/Mo

Second-floor office space with elevator access, near Destin Commons.

View details
Office Suite in Shopping Center
Office Suite in Shopping Center

4300 Legendary Drive C-214, Destin, FL 32541

$4,000/Mo

Office unit located within the Destin Commons complex, accessible from Legendary Drive.

View details
Destin Office Space For Rent
Destin Office Space For Rent

4458 Legendary Drive #240, Destin, FL 32541

$1,474/Mo

Three offices with break room available for rent in Destin.

View details
Freestanding Buildings on Emerald Coast Parkway
Freestanding Buildings on Emerald Coast Parkway

36250 Emerald Coast Parkway #250 & 254, Destin, FL 32541

$18,355/Mo
3,567 sqft $61.75 SF/Yr

Two well-built buildings with excellent visibility on Emerald Coast Parkway.

View details
Destin Office Space Available
Destin Office Space Available

910 Airport Rd, Destin, FL

$14 SF/Yr
1,200 sqft $1,400/Mo

Office space for lease in Destin, Florida.

View details
First-Floor Office Suite Available
First-Floor Office Suite Available

4458 Legendary Drive #100, Destin, FL 32541

$24 SF/Yr

First-floor office suite featuring multiple offices, conference rooms, and amenities.

View details
Versatile Office Space for Rent
Versatile Office Space for Rent

135 Benning Drive, Destin, FL 32541

$18 SF/Yr
5,284 sqft $7,926/Mo

Adaptable office space with finished and unfinished areas.

View details
East Destin Professional Office Space
East Destin Professional Office Space

35008 emerald coast Parkway #203, Destin, FL 32541

$23 SF/Yr
30,000 sqft $57,500/Mo

Professional office space available in East Destin with excellent visibility.

View details
Office Space in Regatta Commons
Office Space in Regatta Commons

4477 Legendary Drive 102, Destin, FL 32541

$2,500/Mo

Office unit for rent in East Destin office park.

View details
East Destin Professional Office Space
East Destin Professional Office Space

35008 emerald coast Parkway #200, Destin, FL 32541

$22 SF/Yr
30,000 sqft $55,000/Mo

Professional office space for lease in prominent East Destin building.

View details
Destin Commerce Center Office Space
Destin Commerce Center Office Space

34990 Emerald Coast Pkwy, Destin, FL 32541

$8 SF/Yr

Office space in Destin Commerce Center, near beach and retail.

View details
East Destin Professional Office Space
East Destin Professional Office Space

35008 emerald coast Parkway #202, Destin, FL 32541

$23 SF/Yr
30,000 sqft $57,500/Mo

Professional office space available for lease in East Destin.

View details
Prime Commercial Space in Destin
Prime Commercial Space in Destin

4460 Legendary Drive, Destin, FL 32541

$26 SF/Yr
7,000 sqft $15,166/Mo

Class A commercial property in Destin, Florida, with high visibility.

View details

Destin, FL Office Spaces Market Trends and Statistics

Explore Office Spaces leasing options in Destin, FL with 32 listings featured on our commercial real estate exchange. The current inventory includes 415,339 square feet of properties with an estimated lease value of $603.32 /Mo.

Estimated lease rates for Office Spaces in Destin, FL begin at $0.74 SF/Yr, with an average of $27.42 SF/Yr and extend to $140.73 SF/Yr.
List
Map