Destin, FL Office buildings for Rent & Lease

Updated: Nov 11, 2025

Freestanding Office Buildings

36250 Emerald Coast Parkway, Destin, FL 32541

$18,355/Mo

3,567 sqft 0.33 AC lot

Two freestanding office buildings totaling 7,343 square feet
Building 250 includes 7 offices, elevator, conference room, storage, and 14 parking spaces
Building 254 includes 6 offices, lobby and reception area, break room, and 9 parking spaces
Located at a signalized intersection at Emerald Coast Parkway and Trista Terrace Court
Large electronic sign visible to 54,000 AADT per day

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Updated: Mar 27

Emerald Coast Parkway Freestanding Buildings

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

$18,355/Mo

3,567 sqft

High visibility location on a hard corner at a signalized intersection with 54,000 AADT.
Two freestanding buildings totaling 7,343 sqft.
Large, HD‑quality electronic marquis sign.
Building 250: 3,567 sqft with 7 offices, 2 Bkrs, ADA bathrooms, elevator, conference room, and 14 parking spaces.
Building 254: 3,776 sqft with lobby & reception area, copy & supply room, ADA bathrooms, 6 offices, break rm, conf, rm, & 9 parking spaces.

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East Destin Professional Office Space

35008 emerald coast Parkway #203, Destin, FL 32541

$23 SF/Yr

120–200 people 30,000 sqft

Professional office space available in East Destin with excellent visibility.

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East Destin Professional Office Space

35008 emerald coast Parkway #200, Destin, FL 32541

$22 SF/Yr

120–200 people 30,000 sqft

Professional office space for lease in prominent East Destin building.

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East Destin Professional Office Space

35008 emerald coast Parkway #202, Destin, FL 32541

$23 SF/Yr

120–200 people 30,000 sqft

Professional office space available for lease in East Destin.

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Two-Story Medical Office Suite

503 Harbor Blvd, Destin, FL 32541

Full service Class A

Contact for pricing

28–46 people 1 space 7,000 sqft 2-story

Two-story professional office suite with an elevator, configured for professional and medical use under a full-service lease.

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Freestanding Office Buildings

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

$18,355/Mo

14–23 people 3,567 sqft Built 2006

Road access

Two separate office buildings offer a range of private offices, meeting rooms, and shared support areas.

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7 active listings match your search: Office Building for lease in Destin, FL. Based on your search, we've also compiled 6 Potential Opportunities for your consideration: 4 spaces in nearby cities and 2 properties for sale.

Office buildings for Lease in Nearby Cities

Here are 4 Similar Spaces we found in Nearby Locations for your consideration.

Freestanding Office Building

4 9th Avenue, Shalimar, FL 32579

$3,542/Mo

10–16 people 2,500 sqft

7 private offices 1 meeting room

Configured for office or medical use with private offices and dedicated reception, meeting, kitchen, and restroom areas.

Reception/filing room Waiting room Kitchen Shower

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Freestanding Corner Medical Office

4 9th Avenue, Shalimar, FL 32579

$4,110/Mo

2,900 sqft

Commercial space across from county services offices, with landlord consideration for tenant-specific remodeling.

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Class A Office Building

511 Government Avenue, Valparaiso, FL 32580

Class A

$33 SF/Yr

494–823 people 123,500 sqft Built 2025 13.47 acres

New professional office space with public dining, landscaped open areas, and a community room near Eglin AFB.

Dining facility Green space Community room

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Under-Construction Office Building

511 Government Avenue, Valparaiso, FL 32580

Class A

$33 SF/Yr

494–823 people 123,500 sqft Built 2025 13.47 acres

Office building under construction with public dining, green space, and a community room.

Ground floor dining facility Green space Community room

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Similar Spaces for Sale in Destin, FL

Consider Similar Space for Sale. We found 2 Spaces matching your search parameters.

Two-Story Office Building

725 Harbor Blvd., Destin, FL 32541

$1,100,000

0.23 AC lot

Flexible professional office layout with separate HVAC systems, dual entrances, and parking on both sides of the building.

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Class A Medical Office Building

4635 Gulfstarr Drive, Destin, FL 32541

$3,399,500

1.10 AC lot

Two-story professional property on a signalized corner with prominent roadside signage.

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Destin, FL Office buildings Lease Rates & Market Statistics

Explore 7 Office buildings for lease in Destin, FL on Realmo, a commercial real estate exchange covering the Destin area. The current inventory totals 107,701 square feet of properties.

Asking lease rates for Office buildings in Destin start at $22 SF/Yr, average $42.21 SF/Yr, and reach $61.75 SF/Yr at the top of the market. That's a 3x spread between entry-level and premium space, making side-by-side comparison of asking rents and lease terms essential. At $42.21 SF/Yr, the local average runs 60% above Florida's state average of $26.31 SF/Yr.

Destin accounts for 24% of the 29 office buildings currently available across Okaloosa County, where nearby markets include Fort Walton Beach and Valparaiso. Office buildings make up 9% of the 75 Office Spaces currently for lease in Destin, with asking rates averaging $42.21 SF/Yr — 70% above the citywide Office Spaces average of $24.83 SF/Yr. Also worth a look for tenants weighing alternatives: Office Units (69 listings) and Medical Office Space (3 listings) elsewhere in the Destin market.

Featured Destin Real Estate Agencies

Realmo connects you with licensed Destin CRE brokers providing property specifications, local market pricing, and commercial transaction underwriting support.

world Impact real estate

4507 Furling Lane #203 Destin, FL 32541

Phone: (850) 225-7000

www.worldimpactrealestate.com

Somers &Company

36164 Emerald Coast Parkway, Suite 8 Destin, FL 32541

Phone: (850) 654-7777

www.somerscompany.com

Taylor Allen Properties LLC

1174 Bay Ct. Destin, FL 32541

Phone: (850) 259-2894

taylorallenllc.com