diff --git a/agent/agentcontainers/api.go b/agent/agentcontainers/api.go
index ce252fe2909ab..1dddcc709848e 100644
--- a/agent/agentcontainers/api.go
+++ b/agent/agentcontainers/api.go
@@ -1099,14 +1099,33 @@ func (api *API) injectSubAgentIntoContainerLocked(ctx context.Context, dc coders
 		directory = DevcontainerDefaultContainerWorkspaceFolder
 	}
 
-	var displayApps []codersdk.DisplayApp
+	displayAppsMap := map[codersdk.DisplayApp]bool{
+		// NOTE(DanielleMaywood):
+		// We use the same defaults here as set in terraform-provider-coder.
+		// https://github.com/coder/terraform-provider-coder/blob/c1c33f6d556532e75662c0ca373ed8fdea220eb5/provider/agent.go#L38-L51
+		codersdk.DisplayAppVSCodeDesktop:  true,
+		codersdk.DisplayAppVSCodeInsiders: false,
+		codersdk.DisplayAppWebTerminal:    true,
+		codersdk.DisplayAppSSH:            true,
+		codersdk.DisplayAppPortForward:    true,
+	}
 
 	if config, err := api.dccli.ReadConfig(ctx, dc.WorkspaceFolder, dc.ConfigPath); err != nil {
 		api.logger.Error(ctx, "unable to read devcontainer config", slog.Error(err))
 	} else {
 		coderCustomization := config.MergedConfiguration.Customizations.Coder
-		if coderCustomization != nil {
-			displayApps = coderCustomization.DisplayApps
+
+		for _, customization := range coderCustomization {
+			for app, enabled := range customization.DisplayApps {
+				displayAppsMap[app] = enabled
+			}
+		}
+	}
+
+	displayApps := make([]codersdk.DisplayApp, 0, len(displayAppsMap))
+	for app, enabled := range displayAppsMap {
+		if enabled {
+			displayApps = append(displayApps, app)
 		}
 	}
 
diff --git a/agent/agentcontainers/api_test.go b/agent/agentcontainers/api_test.go
index d8e696e151db2..821117685b50e 100644
--- a/agent/agentcontainers/api_test.go
+++ b/agent/agentcontainers/api_test.go
@@ -1450,7 +1450,7 @@ func TestAPI(t *testing.T) {
 
 		tests := []struct {
 			name          string
-			customization *agentcontainers.CoderCustomization
+			customization []agentcontainers.CoderCustomization
 			afterCreate   func(t *testing.T, subAgent agentcontainers.SubAgent)
 		}{
 			{
@@ -1458,19 +1458,68 @@ func TestAPI(t *testing.T) {
 				customization: nil,
 			},
 			{
-				name: "WithDisplayApps",
-				customization: &agentcontainers.CoderCustomization{
-					DisplayApps: []codersdk.DisplayApp{
-						codersdk.DisplayAppSSH,
-						codersdk.DisplayAppWebTerminal,
-						codersdk.DisplayAppVSCodeInsiders,
+				name:          "WithDefaultDisplayApps",
+				customization: []agentcontainers.CoderCustomization{},
+				afterCreate: func(t *testing.T, subAgent agentcontainers.SubAgent) {
+					require.Len(t, subAgent.DisplayApps, 4)
+					assert.Contains(t, subAgent.DisplayApps, codersdk.DisplayAppVSCodeDesktop)
+					assert.Contains(t, subAgent.DisplayApps, codersdk.DisplayAppWebTerminal)
+					assert.Contains(t, subAgent.DisplayApps, codersdk.DisplayAppSSH)
+					assert.Contains(t, subAgent.DisplayApps, codersdk.DisplayAppPortForward)
+				},
+			},
+			{
+				name: "WithAllDisplayApps",
+				customization: []agentcontainers.CoderCustomization{
+					{
+						DisplayApps: map[codersdk.DisplayApp]bool{
+							codersdk.DisplayAppSSH:            true,
+							codersdk.DisplayAppWebTerminal:    true,
+							codersdk.DisplayAppVSCodeDesktop:  true,
+							codersdk.DisplayAppVSCodeInsiders: true,
+							codersdk.DisplayAppPortForward:    true,
+						},
+					},
+				},
+				afterCreate: func(t *testing.T, subAgent agentcontainers.SubAgent) {
+					require.Len(t, subAgent.DisplayApps, 5)
+					assert.Contains(t, subAgent.DisplayApps, codersdk.DisplayAppSSH)
+					assert.Contains(t, subAgent.DisplayApps, codersdk.DisplayAppWebTerminal)
+					assert.Contains(t, subAgent.DisplayApps, codersdk.DisplayAppVSCodeDesktop)
+					assert.Contains(t, subAgent.DisplayApps, codersdk.DisplayAppVSCodeInsiders)
+					assert.Contains(t, subAgent.DisplayApps, codersdk.DisplayAppPortForward)
+				},
+			},
+			{
+				name: "WithSomeDisplayAppsDisabled",
+				customization: []agentcontainers.CoderCustomization{
+					{
+						DisplayApps: map[codersdk.DisplayApp]bool{
+							codersdk.DisplayAppSSH:            false,
+							codersdk.DisplayAppWebTerminal:    false,
+							codersdk.DisplayAppVSCodeInsiders: false,
+
+							// We'll enable vscode in this layer, and disable
+							// it in the next layer to ensure a layer can be
+							// disabled.
+							codersdk.DisplayAppVSCodeDesktop: true,
+
+							// We disable port-forward in this layer, and
+							// then re-enable it in the next layer to ensure
+							// that behavior works.
+							codersdk.DisplayAppPortForward: false,
+						},
+					},
+					{
+						DisplayApps: map[codersdk.DisplayApp]bool{
+							codersdk.DisplayAppVSCodeDesktop: false,
+							codersdk.DisplayAppPortForward:   true,
+						},
 					},
 				},
 				afterCreate: func(t *testing.T, subAgent agentcontainers.SubAgent) {
-					require.Len(t, subAgent.DisplayApps, 3)
-					assert.Equal(t, codersdk.DisplayAppSSH, subAgent.DisplayApps[0])
-					assert.Equal(t, codersdk.DisplayAppWebTerminal, subAgent.DisplayApps[1])
-					assert.Equal(t, codersdk.DisplayAppVSCodeInsiders, subAgent.DisplayApps[2])
+					require.Len(t, subAgent.DisplayApps, 1)
+					assert.Contains(t, subAgent.DisplayApps, codersdk.DisplayAppPortForward)
 				},
 			},
 		}
diff --git a/agent/agentcontainers/devcontainercli.go b/agent/agentcontainers/devcontainercli.go
index 2fad8c6560067..002858c70562e 100644
--- a/agent/agentcontainers/devcontainercli.go
+++ b/agent/agentcontainers/devcontainercli.go
@@ -27,11 +27,11 @@ type DevcontainerConfiguration struct {
 }
 
 type DevcontainerCustomizations struct {
-	Coder *CoderCustomization `json:"coder,omitempty"`
+	Coder []CoderCustomization `json:"coder,omitempty"`
 }
 
 type CoderCustomization struct {
-	DisplayApps []codersdk.DisplayApp `json:"displayApps,omitempty"`
+	DisplayApps map[codersdk.DisplayApp]bool `json:"displayApps,omitempty"`
 }
 
 // DevcontainerCLI is an interface for the devcontainer CLI.
diff --git a/agent/agentcontainers/devcontainercli_test.go b/agent/agentcontainers/devcontainercli_test.go
index dfe390ff7e6df..cffb3e12fd494 100644
--- a/agent/agentcontainers/devcontainercli_test.go
+++ b/agent/agentcontainers/devcontainercli_test.go
@@ -258,10 +258,18 @@ func TestDevcontainerCLI_ArgsAndParsing(t *testing.T) {
 				wantConfig: agentcontainers.DevcontainerConfig{
 					MergedConfiguration: agentcontainers.DevcontainerConfiguration{
 						Customizations: agentcontainers.DevcontainerCustomizations{
-							Coder: &agentcontainers.CoderCustomization{
-								DisplayApps: []codersdk.DisplayApp{
-									codersdk.DisplayAppVSCodeDesktop,
-									codersdk.DisplayAppWebTerminal,
+							Coder: []agentcontainers.CoderCustomization{
+								{
+									DisplayApps: map[codersdk.DisplayApp]bool{
+										codersdk.DisplayAppVSCodeDesktop: true,
+										codersdk.DisplayAppWebTerminal:   true,
+									},
+								},
+								{
+									DisplayApps: map[codersdk.DisplayApp]bool{
+										codersdk.DisplayAppVSCodeInsiders: true,
+										codersdk.DisplayAppWebTerminal:    false,
+									},
 								},
 							},
 						},
diff --git a/agent/agentcontainers/testdata/devcontainercli/readconfig/read-config-with-coder-customization.log b/agent/agentcontainers/testdata/devcontainercli/readconfig/read-config-with-coder-customization.log
index fd052c50662e9..d98eb5e056d0c 100644
--- a/agent/agentcontainers/testdata/devcontainercli/readconfig/read-config-with-coder-customization.log
+++ b/agent/agentcontainers/testdata/devcontainercli/readconfig/read-config-with-coder-customization.log
@@ -5,4 +5,4 @@
 {"type":"stop","level":2,"timestamp":1749557820039,"text":"Run: docker ps -q -a --filter label=devcontainer.local_folder=/home/coder/coder --filter label=devcontainer.config_file=/home/coder/coder/.devcontainer/devcontainer.json","startTimestamp":1749557820023}
 {"type":"start","level":2,"timestamp":1749557820039,"text":"Run: docker ps -q -a --filter label=devcontainer.local_folder=/home/coder/coder"}
 {"type":"stop","level":2,"timestamp":1749557820054,"text":"Run: docker ps -q -a --filter label=devcontainer.local_folder=/home/coder/coder","startTimestamp":1749557820039}
-{"mergedConfiguration":{"customizations":{"coder":{"displayApps":["vscode", "web_terminal"]}}}}
+{"mergedConfiguration":{"customizations":{"coder":[{"displayApps":{"vscode":true,"web_terminal":true}},{"displayApps":{"vscode_insiders":true,"web_terminal":false}}]}}}