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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Two-Story Medical Office Suite

503 Harbor Blvd, Destin, FL 32541

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7,000 sqft

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

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East Destin Professional Office Space

35008 emerald coast Parkway #203, Destin, FL 32541

$23 SF/Yr

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

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

30,000 sqft

Professional office space available for lease in East Destin.

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Class A Commercial Building Destin

4460 Legendary Drive, Destin, FL 32541

$24 SF/Yr

14,900 sqft

14,900 SF Class A commercial building for lease in Destin, FL.

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Based on your search, we've compiled 13 Potential Opportunities for your consideration. Besides 7 Active listings in Destin, FL, we suggest exploring alternatives. Consider Similar 4 Spaces in Nearby Cities, and Similar 2 Properties for Sales.

Office buildings for Lease in Nearby Cities

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

Class A Office Building

511 Government Avenue, Valparaiso, FL 32580

$33 SF/Yr

123,500 sqft 13.47 AC lot

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

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Under-Construction Office Building

511 Government Avenue, Valparaiso, FL 32580

$33 SF/Yr

123,500 sqft 13.47 AC lot

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

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Freestanding Office Building

4 9th Avenue, Shalimar, FL 32579

$3,542/Mo

2,500 sqft

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

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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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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 119,034 square feet of properties.

Asking lease rates for Office buildings in Destin start at $22 SF/Yr, average $35.92 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 $35.92 SF/Yr, the local average runs 35% above Florida's state average of $26.55 SF/Yr.

Destin accounts for 30% of the 23 office buildings currently available across Okaloosa County, where nearby markets include Fort Walton Beach and Valparaiso. Office buildings make up 13% of the 53 Office Spaces currently for lease in Destin, with asking rates averaging $35.92 SF/Yr — 57% above the citywide Office Spaces average of $22.84 SF/Yr. Also worth a look for tenants weighing alternatives: Office Units (47 listings) and Medical Office Space (3 listings) elsewhere in the Destin market.