diff --git a/acceptance/bundle/debug/list-targets-root-workspace/databricks.yml b/acceptance/bundle/debug/list-targets-root-workspace/databricks.yml
new file mode 100644
index 00000000000..8732d647fbd
--- /dev/null
+++ b/acceptance/bundle/debug/list-targets-root-workspace/databricks.yml
@@ -0,0 +1,17 @@
+bundle:
+  name: test-bundle
+
+workspace:
+  host: https://custom.test
+  workspace_id: "5678"
+
+targets:
+  inherited:
+    default: true
+  target_query_id:
+    workspace:
+      host: https://custom.test/?o=1234
+  target_workspace_id:
+    workspace:
+      workspace_id: "9012"
+  null_target:
diff --git a/acceptance/bundle/debug/list-targets-root-workspace/out.test.toml b/acceptance/bundle/debug/list-targets-root-workspace/out.test.toml
new file mode 100644
index 00000000000..a927a5fbc06
--- /dev/null
+++ b/acceptance/bundle/debug/list-targets-root-workspace/out.test.toml
@@ -0,0 +1,2 @@
+Cloud = false
+EnvMatrix.DMS = ["", "true"]
diff --git a/acceptance/bundle/debug/list-targets-root-workspace/output.txt b/acceptance/bundle/debug/list-targets-root-workspace/output.txt
new file mode 100644
index 00000000000..176eb4511b4
--- /dev/null
+++ b/acceptance/bundle/debug/list-targets-root-workspace/output.txt
@@ -0,0 +1,33 @@
+
+>>> [CLI] bundle debug list-targets
+inherited (default) https://custom.test workspace_id:5678
+null_target https://custom.test workspace_id:5678
+target_query_id https://custom.test workspace_id:5678
+target_workspace_id https://custom.test workspace_id:9012
+
+>>> [CLI] bundle debug list-targets --output json
+{
+  "targets": [
+    {
+      "name": "inherited",
+      "default": true,
+      "host": "https://custom.test",
+      "workspace_id": "5678"
+    },
+    {
+      "name": "null_target",
+      "host": "https://custom.test",
+      "workspace_id": "5678"
+    },
+    {
+      "name": "target_query_id",
+      "host": "https://custom.test",
+      "workspace_id": "5678"
+    },
+    {
+      "name": "target_workspace_id",
+      "host": "https://custom.test",
+      "workspace_id": "9012"
+    }
+  ]
+}
\ No newline at end of file
diff --git a/acceptance/bundle/debug/list-targets-root-workspace/script b/acceptance/bundle/debug/list-targets-root-workspace/script
new file mode 100644
index 00000000000..fb699dee0cc
--- /dev/null
+++ b/acceptance/bundle/debug/list-targets-root-workspace/script
@@ -0,0 +1,2 @@
+trace $CLI bundle debug list-targets
+trace $CLI bundle debug list-targets --output json
diff --git a/acceptance/bundle/debug/list-targets/databricks.yml b/acceptance/bundle/debug/list-targets/databricks.yml
index 438256ff729..8194820880c 100644
--- a/acceptance/bundle/debug/list-targets/databricks.yml
+++ b/acceptance/bundle/debug/list-targets/databricks.yml
@@ -20,6 +20,17 @@ targets:
     mode: production
     workspace:
       host: https://prod.example.com
+  custom_host_query_id:
+    workspace:
+      host: https://custom.test/?o=1234
+  custom_host_explicit_id:
+    workspace:
+      host: https://custom.test
+      workspace_id: 5678
+  custom_host_explicit_id_over_query:
+    workspace:
+      host: https://custom.test/?o=1234
+      workspace_id: "5678"
   uses_terraform:
     bundle:
       engine: terraform
diff --git a/acceptance/bundle/debug/list-targets/output.txt b/acceptance/bundle/debug/list-targets/output.txt
index abf957e8729..a3bf1d27634 100644
--- a/acceptance/bundle/debug/list-targets/output.txt
+++ b/acceptance/bundle/debug/list-targets/output.txt
@@ -1,5 +1,8 @@
 
 >>> [CLI] bundle debug list-targets
+custom_host_explicit_id https://custom.test workspace_id:5678
+custom_host_explicit_id_over_query https://custom.test workspace_id:5678
+custom_host_query_id https://custom.test workspace_id:1234
 dev (default) development https://dev.example.com
 prod production https://prod.example.com
 staging
@@ -10,6 +13,21 @@ with_vars ${var.target_mode} ${var.target_host}
 >>> [CLI] bundle debug list-targets --output json
 {
   "targets": [
+    {
+      "name": "custom_host_explicit_id",
+      "host": "https://custom.test",
+      "workspace_id": "5678"
+    },
+    {
+      "name": "custom_host_explicit_id_over_query",
+      "host": "https://custom.test",
+      "workspace_id": "5678"
+    },
+    {
+      "name": "custom_host_query_id",
+      "host": "https://custom.test",
+      "workspace_id": "1234"
+    },
     {
       "name": "dev",
       "default": true,
diff --git a/acceptance/bundle/strict_profile_match/list_targets/databricks.yml b/acceptance/bundle/strict_profile_match/list_targets/databricks.yml
new file mode 100644
index 00000000000..2d395eca457
--- /dev/null
+++ b/acceptance/bundle/strict_profile_match/list_targets/databricks.yml
@@ -0,0 +1,14 @@
+bundle:
+  name: strict-profile-match
+
+include:
+  - scripts.yml
+
+workspace:
+  workspace_id: "$WORKSPACE_ID"
+
+targets:
+  inherited_workspace_id:
+    default: true
+    workspace:
+      host: $CUSTOM_HOST/?o=2222222222
diff --git a/acceptance/bundle/strict_profile_match/list_targets/out.test.toml b/acceptance/bundle/strict_profile_match/list_targets/out.test.toml
new file mode 100644
index 00000000000..a927a5fbc06
--- /dev/null
+++ b/acceptance/bundle/strict_profile_match/list_targets/out.test.toml
@@ -0,0 +1,2 @@
+Cloud = false
+EnvMatrix.DMS = ["", "true"]
diff --git a/acceptance/bundle/strict_profile_match/list_targets/output.txt b/acceptance/bundle/strict_profile_match/list_targets/output.txt
new file mode 100644
index 00000000000..03af2d917f0
--- /dev/null
+++ b/acceptance/bundle/strict_profile_match/list_targets/output.txt
@@ -0,0 +1,16 @@
+
+=== list-targets reports the inherited workspace ID
+>>> [CLI] bundle debug list-targets -o json
+{
+  "targets": [
+    {
+      "name": "inherited_workspace_id",
+      "default": true,
+      "host": "[CUSTOM_HOST]",
+      "workspace_id": "[WORKSPACE_ID]"
+    }
+  ]
+}
+=== Authentication uses the same workspace ID
+>>> errcode [CLI] bundle run -t inherited_workspace_id show_auth
+profile=workspace_custom_host host=[CUSTOM_HOST] workspace_id=[WORKSPACE_ID]
diff --git a/acceptance/bundle/strict_profile_match/list_targets/script b/acceptance/bundle/strict_profile_match/list_targets/script
new file mode 100644
index 00000000000..0dc0164c6dd
--- /dev/null
+++ b/acceptance/bundle/strict_profile_match/list_targets/script
@@ -0,0 +1,7 @@
+# The top-level workspace_id takes precedence over ?o= in the target's host, so
+# list-targets must report the workspace ID that authentication uses.
+title "list-targets reports the inherited workspace ID"
+trace $CLI bundle debug list-targets -o json
+
+title "Authentication uses the same workspace ID"
+trace errcode $CLI bundle run -t inherited_workspace_id show_auth
diff --git a/bundle/config/root.go b/bundle/config/root.go
index a64b742630e..bbff6a7f04e 100644
--- a/bundle/config/root.go
+++ b/bundle/config/root.go
@@ -326,6 +326,28 @@ func mergeField(rv, ov dyn.Value, name string) (dyn.Value, error) {
 	return dyn.SetByPath(rv, path, out)
 }
 
+// TargetWorkspace returns the workspace settings of the named target as
+// [Root.MergeTargetOverrides] merges them, without modifying the root.
+func (r *Root) TargetWorkspace(name string) (Workspace, error) {
+	target, err := dyn.GetByPath(r.value, dyn.NewPath(dyn.Key("targets"), dyn.Key(name)))
+	if err != nil {
+		return Workspace{}, err
+	}
+	merged, err := mergeField(r.value, target, "workspace")
+	if err != nil {
+		return Workspace{}, fmt.Errorf("failed to merge target=%s field=workspace: %w", name, err)
+	}
+
+	var w Workspace
+	// Neither the root nor the target sets a workspace section.
+	v := merged.Get("workspace")
+	if !v.IsValid() {
+		return w, nil
+	}
+	err = convert.ToTyped(&w, v)
+	return w, err
+}
+
 func (r *Root) MergeTargetOverrides(name string) error {
 	root := r.value
 	target, err := dyn.GetByPath(root, dyn.NewPath(dyn.Key("targets"), dyn.Key(name)))
diff --git a/cmd/bundle/debug/list_targets.go b/cmd/bundle/debug/list_targets.go
index ebd038da11d..5f8e8e36975 100644
--- a/cmd/bundle/debug/list_targets.go
+++ b/cmd/bundle/debug/list_targets.go
@@ -20,10 +20,11 @@ import (
 )
 
 type targetInfo struct {
-	Name    string      `json:"name"`
-	Default bool        `json:"default,omitempty"`
-	Mode    config.Mode `json:"mode,omitempty"`
-	Host    string      `json:"host,omitempty"`
+	Name        string      `json:"name"`
+	Default     bool        `json:"default,omitempty"`
+	Mode        config.Mode `json:"mode,omitempty"`
+	Host        string      `json:"host,omitempty"`
+	WorkspaceID string      `json:"workspace_id,omitempty"`
 
 	// Engine is only reported for targets that use the removed Terraform engine.
 	Engine engine.EngineType `json:"engine,omitempty"`
@@ -34,27 +35,37 @@ type listTargetsOutput struct {
 }
 
 // collectTargets returns the targets sorted by name. The engine of a target is
-// its own bundle.engine if set, otherwise the top-level bundle.engine.
-func collectTargets(targets map[string]*config.Target, rootEngine engine.EngineType) []targetInfo {
+// its own bundle.engine if set, otherwise the top-level bundle.engine. The host
+// and workspace ID come from the target's workspace merged over the top-level
+// one, normalized the same way authentication normalizes them.
+func collectTargets(cfg *config.Root) ([]targetInfo, error) {
+	targets := cfg.Targets
+	rootEngine := cfg.Bundle.Engine
 	names := slices.Sorted(maps.Keys(targets))
 
 	result := make([]targetInfo, 0, len(names))
 	for _, name := range names {
+		w, err := cfg.TargetWorkspace(name)
+		if err != nil {
+			return nil, err
+		}
+		w.NormalizeHostURL()
+		info := targetInfo{
+			Name:        name,
+			Host:        w.Host,
+			WorkspaceID: w.WorkspaceID,
+		}
+
 		t := targets[name]
 		// YAML decoding can leave a nil entry in the map when a target is
 		// declared with a null value. Skip rather than dereference and panic.
 		if t == nil {
-			result = append(result, targetInfo{Name: name, Engine: terraformOnly(rootEngine)})
+			info.Engine = terraformOnly(rootEngine)
+			result = append(result, info)
 			continue
 		}
-		info := targetInfo{
-			Name:    name,
-			Default: t.Default,
-			Mode:    t.Mode,
-		}
-		if t.Workspace != nil {
-			info.Host = t.Workspace.Host
-		}
+		info.Default = t.Default
+		info.Mode = t.Mode
 		targetEngine := rootEngine
 		if t.Bundle != nil && t.Bundle.Engine != engine.EngineNotSet {
 			targetEngine = t.Bundle.Engine
@@ -62,7 +73,7 @@ func collectTargets(targets map[string]*config.Target, rootEngine engine.EngineT
 		info.Engine = terraformOnly(targetEngine)
 		result = append(result, info)
 	}
-	return result
+	return result, nil
 }
 
 func terraformOnly(e engine.EngineType) engine.EngineType {
@@ -73,7 +84,7 @@ func terraformOnly(e engine.EngineType) engine.EngineType {
 }
 
 // NewListTargetsCommand returns a command that lists all bundle targets
-// with their name, default, mode, workspace host, and (if terraform) engine fields.
+// with their name, default, mode, workspace host and ID, and (if terraform) engine fields.
 func NewListTargetsCommand() *cobra.Command {
 	cmd := &cobra.Command{
 		Use:    "list-targets",
@@ -97,7 +108,10 @@ func NewListTargetsCommand() *cobra.Command {
 			return root.ErrAlreadyPrinted
 		}
 
-		targets := collectTargets(b.Config.Targets, b.Config.Bundle.Engine)
+		targets, err := collectTargets(&b.Config)
+		if err != nil {
+			return err
+		}
 
 		switch root.OutputType(cmd) {
 		case flags.OutputText:
@@ -112,6 +126,9 @@ func NewListTargetsCommand() *cobra.Command {
 				if t.Host != "" {
 					parts = append(parts, t.Host)
 				}
+				if t.WorkspaceID != "" {
+					parts = append(parts, "workspace_id:"+t.WorkspaceID)
+				}
 				if t.Engine != "" {
 					parts = append(parts, "engine:"+string(t.Engine))
 				}