diff --git a/coderd/database/modelqueries.go b/coderd/database/modelqueries.go
index 69bea8d81a..b558bba91e 100644
--- a/coderd/database/modelqueries.go
+++ b/coderd/database/modelqueries.go
@@ -78,7 +78,9 @@ func (q *sqlQuerier) GetAuthorizedTemplates(ctx context.Context, arg GetTemplate
 		arg.Deleted,
 		arg.OrganizationID,
 		arg.ExactName,
+		arg.ExactDisplayName,
 		arg.FuzzyName,
+		arg.FuzzyDisplayName,
 		pq.Array(arg.IDs),
 		arg.Deprecated,
 		arg.HasAITask,
diff --git a/coderd/database/queries.sql.go b/coderd/database/queries.sql.go
index af975247f6..f96f5489c7 100644
--- a/coderd/database/queries.sql.go
+++ b/coderd/database/queries.sql.go
@@ -12230,23 +12230,41 @@ WHERE
 			LOWER(t.name) = LOWER($3)
 		ELSE true
 	END
-	-- Filter by name, matching on substring
+	-- Filter by exact display name
 	AND CASE
 		WHEN $4 :: text != '' THEN
-			lower(t.name) ILIKE '%' || lower($4) || '%'
+			LOWER(t.display_name) = LOWER($4)
+		ELSE true
+	END
+	-- Filter by name, matching on substring
+	AND CASE
+		WHEN $5 :: text != '' THEN
+			lower(t.name) ILIKE '%' || lower($5) || '%'
+		ELSE true
+	END
+	-- Filter by display_name, matching on substring (fallback to name if display_name is empty)
+	AND CASE
+		WHEN $6 :: text != '' THEN
+			CASE
+				WHEN t.display_name IS NOT NULL AND t.display_name != '' THEN
+					lower(t.display_name) ILIKE '%' || lower($6) || '%'
+				ELSE
+					-- Remove spaces if present since 't.name' cannot have any spaces
+					lower(t.name) ILIKE '%' || REPLACE(lower($6), ' ', '') || '%'
+			END
 		ELSE true
 	END
 	-- Filter by ids
 	AND CASE
-		WHEN array_length($5 :: uuid[], 1) > 0 THEN
-			t.id = ANY($5)
+		WHEN array_length($7 :: uuid[], 1) > 0 THEN
+			t.id = ANY($7)
 		ELSE true
 	END
 	-- Filter by deprecated
 	AND CASE
-		WHEN $6 :: boolean IS NOT NULL THEN
+		WHEN $8 :: boolean IS NOT NULL THEN
 			CASE
-				WHEN $6 :: boolean THEN
+				WHEN $8 :: boolean THEN
 					t.deprecated != ''
 				ELSE
 					t.deprecated = ''
@@ -12255,27 +12273,27 @@ WHERE
 	END
 	-- Filter by has_ai_task in latest version
 	AND CASE
-		WHEN $7 :: boolean IS NOT NULL THEN
-			tv.has_ai_task = $7 :: boolean
+		WHEN $9 :: boolean IS NOT NULL THEN
+			tv.has_ai_task = $9 :: boolean
 		ELSE true
 	END
 	-- Filter by author_id
 	AND CASE
-		  WHEN $8 :: uuid != '00000000-0000-0000-0000-000000000000'::uuid THEN
-			  t.created_by = $8
+		  WHEN $10 :: uuid != '00000000-0000-0000-0000-000000000000'::uuid THEN
+			  t.created_by = $10
 		  ELSE true
 	END
 	-- Filter by author_username
 	AND CASE
-		  WHEN $9 :: text != '' THEN
-			  t.created_by = (SELECT id FROM users WHERE lower(users.username) = lower($9) AND deleted = false)
+		  WHEN $11 :: text != '' THEN
+			  t.created_by = (SELECT id FROM users WHERE lower(users.username) = lower($11) AND deleted = false)
 		  ELSE true
 	END
 
 	-- Filter by has_external_agent in latest version
 	AND CASE
-		WHEN $10 :: boolean IS NOT NULL THEN
-			tv.has_external_agent = $10 :: boolean
+		WHEN $12 :: boolean IS NOT NULL THEN
+			tv.has_external_agent = $12 :: boolean
 		ELSE true
 	END
   -- Authorize Filter clause will be injected below in GetAuthorizedTemplates
@@ -12287,7 +12305,9 @@ type GetTemplatesWithFilterParams struct {
 	Deleted          bool         `db:"deleted" json:"deleted"`
 	OrganizationID   uuid.UUID    `db:"organization_id" json:"organization_id"`
 	ExactName        string       `db:"exact_name" json:"exact_name"`
+	ExactDisplayName string       `db:"exact_display_name" json:"exact_display_name"`
 	FuzzyName        string       `db:"fuzzy_name" json:"fuzzy_name"`
+	FuzzyDisplayName string       `db:"fuzzy_display_name" json:"fuzzy_display_name"`
 	IDs              []uuid.UUID  `db:"ids" json:"ids"`
 	Deprecated       sql.NullBool `db:"deprecated" json:"deprecated"`
 	HasAITask        sql.NullBool `db:"has_ai_task" json:"has_ai_task"`
@@ -12301,7 +12321,9 @@ func (q *sqlQuerier) GetTemplatesWithFilter(ctx context.Context, arg GetTemplate
 		arg.Deleted,
 		arg.OrganizationID,
 		arg.ExactName,
+		arg.ExactDisplayName,
 		arg.FuzzyName,
+		arg.FuzzyDisplayName,
 		pq.Array(arg.IDs),
 		arg.Deprecated,
 		arg.HasAITask,
diff --git a/coderd/database/queries/templates.sql b/coderd/database/queries/templates.sql
index 05b663aca4..43f1aea6c5 100644
--- a/coderd/database/queries/templates.sql
+++ b/coderd/database/queries/templates.sql
@@ -30,12 +30,30 @@ WHERE
 			LOWER(t.name) = LOWER(@exact_name)
 		ELSE true
 	END
+	-- Filter by exact display name
+	AND CASE
+		WHEN @exact_display_name :: text != '' THEN
+			LOWER(t.display_name) = LOWER(@exact_display_name)
+		ELSE true
+	END
 	-- Filter by name, matching on substring
 	AND CASE
 		WHEN @fuzzy_name :: text != '' THEN
 			lower(t.name) ILIKE '%' || lower(@fuzzy_name) || '%'
 		ELSE true
 	END
+	-- Filter by display_name, matching on substring (fallback to name if display_name is empty)
+	AND CASE
+		WHEN @fuzzy_display_name :: text != '' THEN
+			CASE
+				WHEN t.display_name IS NOT NULL AND t.display_name != '' THEN
+					lower(t.display_name) ILIKE '%' || lower(@fuzzy_display_name) || '%'
+				ELSE
+					-- Remove spaces if present since 't.name' cannot have any spaces
+					lower(t.name) ILIKE '%' || REPLACE(lower(@fuzzy_display_name), ' ', '') || '%'
+			END
+		ELSE true
+	END
 	-- Filter by ids
 	AND CASE
 		WHEN array_length(@ids :: uuid[], 1) > 0 THEN
diff --git a/coderd/searchquery/search.go b/coderd/searchquery/search.go
index 9748729736..0ab700fbee 100644
--- a/coderd/searchquery/search.go
+++ b/coderd/searchquery/search.go
@@ -268,8 +268,8 @@ func Templates(ctx context.Context, db database.Store, actorID uuid.UUID, query
 	// Always lowercase for all searches.
 	query = strings.ToLower(query)
 	values, errors := searchTerms(query, func(term string, values url.Values) error {
-		// Default to the template name
-		values.Add("name", term)
+		// Default to the display name
+		values.Add("display_name", term)
 		return nil
 	})
 	if len(errors) > 0 {
@@ -281,7 +281,9 @@ func Templates(ctx context.Context, db database.Store, actorID uuid.UUID, query
 		Deleted:          parser.Boolean(values, false, "deleted"),
 		OrganizationID:   parseOrganization(ctx, db, parser, values, "organization"),
 		ExactName:        parser.String(values, "", "exact_name"),
+		ExactDisplayName: parser.String(values, "", "exact_display_name"),
 		FuzzyName:        parser.String(values, "", "name"),
+		FuzzyDisplayName: parser.String(values, "", "display_name"),
 		IDs:              parser.UUIDs(values, []uuid.UUID{}, "ids"),
 		Deprecated:       parser.NullableBoolean(values, sql.NullBool{}, "deprecated"),
 		HasAITask:        parser.NullableBoolean(values, sql.NullBool{}, "has-ai-task"),
@@ -305,7 +307,8 @@ func searchTerms(query string, defaultKey func(term string, values url.Values) e
 	// Because we do this in 2 passes, we want to maintain quotes on the first
 	// pass. Further splitting occurs on the second pass and quotes will be
 	// dropped.
-	elements := splitQueryParameterByDelimiter(query, ' ', true)
+	tokens := splitQueryParameterByDelimiter(query, ' ', true)
+	elements := processTokens(tokens)
 	for _, element := range elements {
 		if strings.HasPrefix(element, ":") || strings.HasSuffix(element, ":") {
 			return nil, []codersdk.ValidationError{
@@ -385,3 +388,24 @@ func splitQueryParameterByDelimiter(query string, delimiter rune, maintainQuotes
 
 	return parts
 }
+
+// processTokens takes the split tokens and groups them based on a delimiter (':').
+// Tokens without a delimiter present are joined to support searching with spaces.
+//
+//	Example Input: ['deprecated:false', 'test', 'template']
+//	Example Output: ['deprecated:false', 'test template']
+func processTokens(tokens []string) []string {
+	var results []string
+	var nonFieldTerms []string
+	for _, token := range tokens {
+		if strings.Contains(token, string(':')) {
+			results = append(results, token)
+		} else {
+			nonFieldTerms = append(nonFieldTerms, token)
+		}
+	}
+	if len(nonFieldTerms) > 0 {
+		results = append(results, strings.Join(nonFieldTerms, " "))
+	}
+	return results
+}
diff --git a/coderd/searchquery/search_test.go b/coderd/searchquery/search_test.go
index 2a8f4cd6cb..5c52e15851 100644
--- a/coderd/searchquery/search_test.go
+++ b/coderd/searchquery/search_test.go
@@ -686,7 +686,7 @@ func TestSearchTemplates(t *testing.T) {
 			Name:  "OnlyName",
 			Query: "foobar",
 			Expected: database.GetTemplatesWithFilterParams{
-				FuzzyName: "foobar",
+				FuzzyDisplayName: "foobar",
 			},
 		},
 		{
@@ -757,6 +757,43 @@ func TestSearchTemplates(t *testing.T) {
 				AuthorID:       userID,
 			},
 		},
+		{
+			Name:  "SearchOnDisplayName",
+			Query: "test name",
+			Expected: database.GetTemplatesWithFilterParams{
+				FuzzyDisplayName: "test name",
+			},
+		},
+		{
+			Name:  "NameField",
+			Query: "name:testname",
+			Expected: database.GetTemplatesWithFilterParams{
+				FuzzyName: "testname",
+			},
+		},
+		{
+			Name:  "QuotedValue",
+			Query: `name:"test name"`,
+			Expected: database.GetTemplatesWithFilterParams{
+				FuzzyName: "test name",
+			},
+		},
+		{
+			Name:  "MultipleTerms",
+			Query: `foo bar exact_name:"test display name"`,
+			Expected: database.GetTemplatesWithFilterParams{
+				ExactName:        "test display name",
+				FuzzyDisplayName: "foo bar",
+			},
+		},
+		{
+			Name:  "FieldAndSpaces",
+			Query: "deprecated:false test template",
+			Expected: database.GetTemplatesWithFilterParams{
+				Deprecated:       sql.NullBool{Bool: false, Valid: true},
+				FuzzyDisplayName: "test template",
+			},
+		},
 	}
 
 	for _, c := range testCases {